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Grazing impact of copepods on phytoplankton in the Bohai Sea
Estuarine, Coastal and Shelf Science 58 (2003) 487–498
Grazing impact of copepods on phytoplankton in the Bohai Sea Chaolun Li*, Rong Wang, Song Sun Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, People’s Republic of China Received 2 May 2002; accepted 24 April 2003
Abstract During spring (April/May 1999) and autumn (September/October 1998) cruises in the Bohai Sea, China, copepods were the dominant components of mesozooplankton, the most abundant species being Calanus sinicus, Centropages mcmurrichi, Paracalanus parvus, Acartia bifilosa and Oithona similis. Pigment ingestion rates by three size classes of copepods (200–500, 500–1000 and >1000 lm) were measured. In the south of the investigation area, gut pigment content (GPC), individual pigment-specific ingestion rates and grazing impacts on phytoplankton were lower in spring than in autumn. In the central area, GPC and individual pigmentspecific ingestion rates were higher in spring than in autumn. The grazing impact on phytoplankton by the copepod assemblages was lower in spring than in autumn, however, because of the relatively smaller biomass in spring. In the western area where the Bohai Sea joins the Yellow Sea, GPC, individual pigment-specific ingestion rates and grazing impacts on phytoplankton were higher in spring than in autumn. Among the three size groups, the small-sized animals (200–500 lm) contributed more than 50% (range 38–98%) of the total copepod grazing during both cruises. The grazing impact on phytoplankton by copepods was equivalent to 11.9% (range 3.0– 37.1%) of the chlorophyll-a standing stock and 53.3% (range 21.4–91.4%) of the primary production during the spring cruise. Grazing impact was equivalent to 6.3% (range 2.0–11.6%) of the chlorophyll-a standing stock and >100% (range 25.7–141.6%) of the primary production during the autumn cruise. The copepod community apparently consumed only a modest proportion of the standing stock of phytoplankton during spring and autumn blooms. They did, however, sometimes graze a significant proportion of daily primary production and hence were presumably able to limit the rate of further accumulation of phytoplankton, or even to prevent it. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: copepod; feeding; Bohai Sea
1. Introduction Zooplankton, an integral component of the food web, links phytoplankton production and production of fishes and other animals at higher trophic levels in marine ecosystems. As the GLOBEC Implementation Plan (1999) indicated, ‘‘Reproduction, growth and mortality rates are the essential components of zooplankton population dynamics. The first two of these are under
* Corresponding author. E-mail address: [email protected] (C. Li). 0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(03)00129-X
the direct influence of feeding. Hence studies on feeding of zooplankton are important to advance our understanding of ocean ecosystem dynamics.’’ The emphasis of research on the grazing impact of marine mesozooplankton on phytoplankton has usually been on older stages and larger taxa. Recently, more and more studies have indicated, however, that smaller copepods may often play a more important role than the larger animals not only in terms of abundance, but also in terms of biomass and grazing pressure on the phytoplankton (e.g. Dam & Peterson, 1993; Morales, Bedo, Harris, & Tranter, 1991; Zhang, Dam, White, & Roman, 1995). Studies on feeding in small copepods have been limited, however, because of the diversity of
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Fig. 1. Location of Bohai Sea.
species and developmental stages amongst these smaller taxa. Over the last decade, a body-size approach has been reported as the simplest and most reliable method of dealing with this problem and has been used to estimate the importance of different size fractions in the consumption of phytoplankton (Barquero et al., 1998; Dam, Zhang, Butler, & Roman, 1995; Morales et al., 1991; Williams & Conway, 1988; Zhang et al., 1995). This approach is also appropriate in the sense that this type of ecosystem study should be able to provide order of magnitude estimates as a starting basis for modeling the dynamics within a system (Li & Wang, 2000; Morales et al., 1991). The Bohai Sea is a semi-closed shallow embayment in China with an area of 77,000 km2 (Fig. 1). During the past decades, aquaculture, sea farming and changes in inputs of freshwater, nutrients and sediments have resulted in changes in structure and function of the marine ecosystem. Thus, the Bohai Sea was chosen as one of the China-GLOBEC study areas. One of the components of the project is a study of the feeding of herbivorous copepods in order to improve our understanding of the marine trophic dynamics in this area. This paper presents the seasonal and spatial patterns of size-fractionated copepod grazing in the Bohai Sea, and evaluates the importance of different groups of copepods in terms of their grazing impact on phytoplankton standing stock and primary production.
phytoplankton (Fig. 1). In the autumn cruise, stations A4 and B1 were only occupied for 12 h and E1 was cancelled because of bad weather. Hydrographic conditions and concentrations of chlorophyll-a in each station are shown in Table 1. 2.1. Sampling Zooplankton samples were collected by a net with mouth area of 0.5 m2 and mesh size of 200 lm towed vertically from the bottom to the surface. A flowmeter (T. S. K. made in Japan) was mounted in the center of the mouth of the net to measure the volume of water filtered. Samples were preserved in a 5% formalin– seawater solution. In the laboratory, the entire contents of each sample were sieved through 1000, 500 and 200 lm mesh to divide it into three size fractions. Under a dissecting microscope, 100% of the large, 50–100% of the medium and 10–50% of the small fractions were examined, and the number of copepods was enumerated. Day/night pairs of samples for mesozooplankton abundance were taken at all stations. The mean value of two samples at same station was used to calculate mesozooplankton abundance. Samples for gut pigment analysis and gut evacuation experiments were captured using the same net but with a sealed cod end. 2.2. Gut pigment analysis of zooplankton
2. Materials and methods Two survey cruises were carried out in the Bohai Sea during the spring (April/May 1999) and autumn (October/November 1998). Five stations, where the ship was anchored for 27–30 h, were chosen to study the copepod feeding activities and grazing impact on
Immediately after sampling, the cod-end contents were poured into soda/seawater solution (1 : 5, v/v) to anaesthetize the animals (Kleppel, Frazel, Pieper, & Holliday, 1988), then sieved through 1000, 500 and 200 lm mesh and gently rinsed with filtered seawater to wash away coarse phytoplankton cells. The resultant fractions were sorted under dim light and about 20
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C. Li et al. / Estuarine, Coastal and Shelf Science 58 (2003) 487–498 Table 1 The temperature and chlorophyll-a conditions of survey stations during the study periodsa Temperature ( C)
Chlorophyll-a (mg m3)
Station
Date
Depth (m)
Surface
Bottom
Surface
Bottom
Depth of maximumb
A2
1–2 May 27–28 September 2–3 May 6 October 6–7 May 2–3 October 5–6 May 4–5 May 28–29 September
35
8.8–8.8 22.2–22.7 8.6–9.1 21.7–21.8 11.3–12.1 23.4–23.5 10.3–11.3 8.3–8.8 22.8–23.5
6.7–6.9 20.6–21.8 6.4–6.5 13.9–14.4 11.3–12.0 23.4–23.6 9.8–10.7 7.9–8.1 22.7–22.8
0.22 1.48 0.33 0.44 2.90 2.12 1.39 1.68 1.31
0.98 0.72 0.75 0.35 3.30 1.63 1.83 3.03 0.86
Bottom 10 m (2.03) Bottom 10 m (0.65) Bottom Bottom Bottom Bottom 10 m (1.82)
A4 B1 E1 E3
50 16 19 26
a
Temperatures were measured with a Sea-Bird SBE 9 CTD (H. Wei, personal communication). Chlorophyll-a concentrations were the average values over a daily cycle (J. Sun, personal communication). b The values in the brackets are the concentrations of chlorophyll-a.
animals of the large fraction, 40 of the medium fraction and 80–100 of the small fraction were individually picked and placed in a 10 ml glass centrifuge tube to which 2–3 ml of 90% acetone solution was added. This operation took about 5–10 min. The tube was capped and stored in dark and kept at 30 C. After finishing the whole sampling of one station, the contents of each tube were homogenized in a glass grinder, transferred back to the centrifuge tube, diluted to 10 ml with 90% acetone solution and extracted in dark at 30 C for 24 h. The tubes were then centrifuged for 10 min and the fluorescence of the suspension from each tube was measured before and after acidification with 10% HCl using a Turner Designs model II. Absolute values for chlorophyll-a and phaeopigments were calculated according to Wang and Conover (1986). The sum was used as the index of gut pigment content (GPC). An empirical equation, C ¼ 50chl, was used to convert chlorophyll-a into phytoplankton carbon. 2.3. Diurnal variation in gut pigment content Diurnal variations in GPC were investigated at anchor stations to study the copepod diurnal feeding rhythms. At each station, samples were collected at 3-h intervals for a complete daily cycle and the GPC was measured as above. The night was defined as the time from sunset to sunrise. The amplitude of feeding rhythms of copepods was estimated by the quotient of night/day (N/D) mean GPC. 2.4. Determination of gut evacuation and ingestion rates of copepods Within 5–10 min after capture, living samples for experiments were gently rinsed with filtered seawater to wash away phytoplankton cells and placed in several beakers (2l in number). The beakers contained 0.45 lm filtered seawater to which non-fluorescent charcoal powder (100 lm diameter) was added to keep the
animals under continuous feeding conditions (Willason & Cox, 1987). Beakers were kept in dark submerged in a constant-temperature water bath set to the surface seawater temperature. Initially, and after 10, 20, 30, 60, 90 and 120 min, animals were taken from the respective containers, put into the glass centrifuge tube to which 2–3 ml of 90% acetone solution was added and frozen at 30 C. Subsequent treatments and measurements were the same as the gut pigment analysis. The gut evacuation rate constant (k) was calculated by using a negative exponential equation (Mackas & Bohrer, 1976). Assuming that the animals were feeding at a constant rate, ingestion rates (I) were calculated from the expression I ¼ GPC k where GPC is the average value over a daily cycle. 2.5. Measurements of gut pigment destruction According to Perissinotto and Pakhomov (1996), a two-compartment pigment budget approach was employed to estimate the gut pigment destruction of the copepods at station B1 during the autumn cruise. Freshly collected large-sized copepods (>1000 lm) were allowed to empty their gut pigment for 24 h in filtered seawater with charcoal powder. Several copepods (20– 30 individuals) were then incubated for 30 min in 500 ml bottles filled with natural seawater sampled from 5 m depth. Comparing the decrease in pigment content in the grazing bottles with the increase in GPC of animals incubated in these bottles, any significant loss of the pigments from the experiment treatments was then attributed to gut destruction of the phytoplankton pigments. The gut pigment degradation efficiencies were calculated using the equation b ð%Þ ¼ f1 ½ðGe Pb Þ= Pg100, where Ge is the individual GPC at the end of the incubation, Pb the individual background fluorescence and P is the total amount of individual pigment ingested (Perissinotto & Pakhomov, 1998).
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Table 2 Abundance of potentially herbivorous copepods and dominant species in the Bohai Sea Station
Season
Large (ind. m3)
Species
Medium (ind. m3)
Species
Small (ind. m3)
Species
A2
Spring
107
C. sinicus
408
C. sinicus C. mcmurrichi
1343
Autumn
12
C. sinicus
9
C. teuniremis T. forcipatus
3906
A. bifilosa O. similis C. affinis P. parvus O. similis C. affinis
Spring
46
C. sinicus
3146
5959
Autumn
91
C. sinicus
101
C. C. C. C.
B1
Spring
167
C. sinicus
283
C. sinicus
Autumn
28
C. sinicus
2
C. sinicus
5053
A. bifilosa P. parvus P. parvus
E1
Spring
26
C. sinicus
31
C. sinicus
9022
A. bifilosa
E3
Spring
35
C. sinicus
269
C. sinicus
2483
Autumn
119
C. sinicus
4
T. forcipatu C. teuniremis
10,418
A. bifilosa P. parvus P. parvus O. similis
A4
3. Results 3.1. Zooplankton composition and distribution Concentrations of copepods in the different size fractions and the identities of constituent species are shown in Table 2. Some species occurred in more than one size group because different developmental stages were present. During the spring cruise, the most abundant species in the large-sized group (>1000 lm) was Calanus sinicus. Centropages mcmurrichi represented >72% of the medium-sized group (500–1000 lm). The small-sized group (200–500 lm) was mainly composed of Acartia bifilosa, Paracalanus parvus, Oithona similis and
sinicus mcmurrichi sinicus teuniremis
A. bifilosa O. similis P. parvus O. similis C. affinis
988
23,987
Corycaeus affinis. During the autumn cruise, C. sinicus was also the abundant species in the large-sized group and the same species were present in the small-sized group as those present during the spring cruise. For the medium-sized group, C. mcmurrichi was almost absent, and Centropages teuniremis and Tortanus forcipatus became the dominant species. The small-sized copepods outnumbered the other groups during both cruises.
3.2. Gut pigment contents Results of the copepod GPC are shown in Table 3. Copepod GPC were higher in spring than in autumn
Table 3 The GPC (ng pigm. ind.1) of copepods in the Bohai Sea in 1998/1999 Spring
Autumn
Station
Size
Mean GPC SD
A2
Large Medium Small
No data No data No data
Mean GPC SD
Chl a : Pha
n
2.095 1.822 0.886 0.392 0.565 0.143
0.24 0.27 0.29
9 9 9
A4
Large Medium Small
No data 1.840 1.506 0.485 0.382
0.24 0.23
9 9
1.193 0.303 0.948 0.241 0.438 0.076
0.35 0.31 0.26
5 5 5
B1
Large Medium Small
1.696 0.589 1.132 0.407 0.305 0.138
0.21 0.29 0.21
9 9 9
4.499 2.094 3.172 1.630 1.275 0.175
0.29 0.43 0.34
5 5 5
E1
Large Medium Small
5.500 1.855 1.348 0.806 0.308 0.115
0.16 0.20 0.31
9 9 9
No data No data No data
E3
Large Medium Small
4.619 2.161 2.774 1.370 0.579 0.211
0.21 0.18 0.16
9 9 9
1.424 0.826 0.906 0.345 0.560 0.091
0.23 0.14 0.19
9 9 9
Chl a : Pha
n
C. Li et al. / Estuarine, Coastal and Shelf Science 58 (2003) 487–498
within the middle and mouth stations of the Bohai Sea (stations A4 and E3, Mann–Whitney U-test, p < 0:1). But within the southern station (B1), GPC for all three size groups were higher in autumn than in spring (Mann–Whitney U-test, p < 0:1). During the spring cruise, for large- and medium-sized groups, the maximum of GPC values of copepod was found at station E1 and the lowest values were found at station B1. In spring, small-sized groups had higher values at stations A4 and E3 than at stations E1 and B1 (Mann–Whitney U-test, p < 0:1). During the autumn cruise, the spatial distribution patterns were similar in all three groups. For all size groups, the values of GPC at station B1 were higher than those at other stations (Mann–Whitney U-test, p < 0:1). The diel cycle of GPC of copepods was observed at four stations (A4, B1, E1 and E3) during the spring cruise (Fig. 2a). Diurnal variations in GPC were different amongst size classes and stations. During the spring cruise, both medium- and small-sized animals showed strong diel feeding rhythms at station A4 with peak GPC values at 23:00 hours. The N/D ratios of GPC were 5.7 for the medium-sized and 4.1 for the small-sized copepods. At station B1, for both large- and medium-sized animals, the mean GPC was also higher at night than during the day. There were two high values of gut pigments during a day, however one at 17:00 hours; and the other at 5:00 hours. For the small-sized group, GPC was lower at night and the peak value occurred at 14:00 hours. At station E1, the diel variations of GPC were the same as that at station B1, with higher values for the large- and medium-sized groups and lower values for the small-sized groups at night. The diel feeding patterns of animals at station E3 were similar to those at station A4, but the changes of the GPC were not as large as those at station A4. The N/D ratios of GPC were only 1.3 for large-sized, 1.6 for medium-sized and 1.4 for small-sized copepods. During the autumn cruise, diel variation in GPC was observed only at two stations (A2 and E3). The diel feeding activities of the animals showed the same patterns at both stations. The large- and medium-sized animals fed more actively at night than during the day. The amplitudes of diel feeding rhythms at A2 (N/D ratios were 3.6 for large-sized and 1.6 for medium-sized animals) were higher than those at E3 (N/D ratio was 1.2 for both large- and medium-sized animals). The levels of GPC for the small-sized animals varied insignificantly during a diel cycle, with N/D ratios of about 0.9–1.1.
3.3. Gut evacuation and ingestion rates Eleven gut evacuation experiments were carried out during spring cruise and 12 during autumn cruise (Table 4). Gut evacuation rate constants showed no trend with
491
temperature or body size. The mean gut evacuation rate constant was 0.0174 min1 during the spring cruise and 0.0161 min1 during the autumn cruise. Four culture experiments were carried out to estimate the levels of gut pigment degradation at station B1 during the autumn cruise (Table 5). The gut pigment destruction degree of large-sized copepods was on average 13%, ranging from 0 to 37%. Considering the great differences in water temperatures, chlorophyll-a concentrations, and copepod abundances and compositions, we did not use this result to rectify the ingestion rate, and just used it as a factor to estimate the accuracy of the gut fluorescence method in our study. Daily individual pigment-specific ingestion rates are shown in Table 4. Individual ingestion rates during spring cruise were higher than those measured during autumn cruise for large- and medium-sized groups. The opposite was true for the small-sized animals. Individual ingestion rates at the center (station E3) and mouth (station A4) of the Bohai Sea were higher than those in the coastal area in spring. In autumn, the maximal values were found at station B1.
3.4. Grazing impact Daily grazing rates were calculated from the data on GPC and evacuation rate constants, and then converted to the ratios for the population in the water column from bottom to surface using the population density. The small-sized animals (200–500 lm) were the dominant grazers at most stations during both cruises, except at station B1 during the spring cruise. They contributed more than 60% (range 33.8–88.9%) to the total copepod community grazing during the spring cruise and 80% (range 66.9–97.5%) during the autumn cruise (Fig. 3). The daily grazing rates of the total copepod communities were on average 2.97 mg pigm. m2 day1 (range 0.99–9.44 mg pigm. m2day1) during the spring cruise and 2.10 mg pigm. m2day1 (range 0.57–4.07 mg pigm. m2day1) during the autumn cruise (Table 6). With respect to the in situ phytoplankton biomass, the daily grazing pressure of copepod communities accounted for 11.9% (range 3.2–37.1%) and 5.1% (range 2.0–8.9%) of the total chlorophyll-a standing stocks during spring and autumn cruises, respectively. Assuming a carbon-to-chlorophyll-a ratio of 50, the average carbon-specific grazing rates of copepod communities were calculated as 173 mg C m2day1 (range 50–472 mg C m2day1) during the spring cruise and 105 mg C m2day1 (range 28–204 mg C m2day1) during the autumn cruise (Table 4). The daily consumption of copepod communities was equivalent to an average of 53.3% (range 24.7–96.4%) and 86.5% (range 25.7– 141.4%) of primary production during spring and autumn cruises, respectively.
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Fig. 2. (a) Diurnal variation in GPC of copepods in the Bohai Sea during the spring cruise. (b) Diurnal variation in GPC of copepods in the Bohai Sea during the autumn cruise.
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C. Li et al. / Estuarine, Coastal and Shelf Science 58 (2003) 487–498 Table 4 The results of the experiments to evaluate gut evacuation rate (GER) and individual ingestion rate in the Bohai Sea during the study periods GER (min1)
Individual ingestion rate (ng pigm. ind.1day1)
Season
Station
Temperature ( C)
Large
Medium
Small
Large
Medium
Spring
A4 B1 E1 E3
7.3 11.3 10.3 8.1
No data 0.0250 0.0250 0.0250
0.0203 0.0161 0.0161 0.0154
0.0138 0.0114 0.0114 0.0114
No data 61.1 207.6 259.6
53.8 26.3 31.3 61.4
9.6 5.0 5.0 9.5
176.1 102.9
43.2 17.0
7.3 2.6
91.4 23.5 113.7 30.6
31.1 14.9 72.5 17.2
10.8 7.3 20.6 13.4
33.9 26.7
13.0 2.6
Mean SD Autumn
0.0174 0.0056 A2 A4 B1 E3
22.1 18.7 23.4 22.8
Mean SD
0.0303 0.0139 0.0175 0.0149
0.0244 0.0106 0.0159 0.0132
0.0161 0.0058
4. Discussion 4.1. The gut fluorescence method The gut fluorescence method is currently one of the most available approaches to measure in situ grazing rates of herbivorous zooplankton. One inaccuracy of this method, however, is that pigment destruction occurs during gut passage and that the degree of pigment destruction varies greatly (Cary, Lovette, Perl, Huntley, & Vernet, 1992; Head & Harris, 1992, 1996; Lopez, Huntley, & Sykes, 1988; McLeroy-Etheridge & McManus, 1999; Penry & Frost, 1991; Stevens & Head, 1998; Wang & Conover, 1986). In the present study, culture experiments at station B1 were conducted to estimate the gut pigment destruction degree of large-sized copepods in the autumn cruise. The results showed that the pigment loss ranged from no degradation to 37% (13% on average; Table 5), which was in the data range reported in some previous results obtained in situ or in the laboratory (Head & Harris, 1996; Landry, Lorenzen, & Peterson, 1994; Landry, Peterson, & Fagerness, 1994; Penry & Frost, 1991). The degree of pigment destruction was related to several factors, including ingestion rate, zooplankton behavior, ambient conditions and the prior feeding history (Head & Harris, 1992, 1996; Penry & Frost, 1991; Stevens & Head, 1998; Tirelli & Mayzaud, 1998). Instead of being starved in the filtered seawater, copepods were fed only charcoal particles for 24 h to clear their guts of fluorescence before the culture
0.0133 0.0116 0.0112 0.0167
64.8 44.6
Small
experiments in this study. This should keep the filterfeeder copepods under active feeding conditions, with particle ingestion and faecal egestion proceeding uninterruptedly (Perissinotto & Pakhomov, 1996; Willason & Cox, 1987). Thereby, it is possible that the present results represented a situation much closer to in situ conditions. Because the concentrations of chlorophylla and copepod ingestion rates were greatly different amongst the stations, it was improper to use the results of station B1 to rectify the ingestion rates of all stations. However, the average value of GPC degradation rates of station B1 (13%) agreed with the idea in Harris’ (1996) review that pigment destruction rates are low (<20%) in the chlorophyll range that most animals will experience in nature, so high pigment loss may not be such a significant factor in the natural environment. Therefore, it is suggested that our measurements of GPC were not underestimated by more than 20%. This underestimation would not change the general conclusions of this paper. Another possible inaccuracy of the gut fluorescence method is associated with the determination of the gut evacuation rate constant. Several factors may affect the results of the gut evacuation experiments, such as the temperature, initial gut content, duration of experiment, incubation in filtered seawater and the intrinsic feeding rhythms (Dam & Peterson, 1988; Head, 1988; Tirelli & Mayzand, 1998; Wang & Conover, 1986). In this investigation, the individuals for gut evacuation experiment were incubated in the filtered seawater with charcoal powder (100 lm diameter) added to keep
Table 5 Estimation of pigment destruction efficiency for large copepods at Station B1 during the autumn cruise Experiment number
Chlorophyll-a concentration (mg m3)
Pigment ingested (ng pigm. ind1)
Pigment recovered (ng pigm. ind.1)
Destruction efficiency (%)
1 2 3 4
1.97 3.94 1.76 2.23
5.58 0.83 6.61 0.92 7.65 4.93 2.34 0.33
5.27 0.91 6.72 1.12 4.85 3.95 1.92 0.42
5.5 3.5 0a 36.5 12.6 18.8 6.4
a
Considering the limits of error, the pigment destruction efficiency in experiment 2 is 0%.
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Fig. 3. Percentage contribution to the total grazing by 200–500, 500–1000 and >1000 lm copepods.
the animals under continuous feeding conditions, and the experiments lasted for 90–120 min, attempting to represent a situation closer to in situ condition. The results confirmed that the gut evacuation rate constants were independent of body size, which has been verified in previous studies (Morale, Bautista, & Harris, 1990; Zhang et al., 1995). Temperature was considered to have the dominant influence on gut evacuation rate constant and an empirical model has been proposed to define their relationship (Dam & Peterson, 1988). Field results showed no relationship between the temperature and
the gut evacuation rate in our study, however. There was no obvious difference between the two seasons, even though the seawater temperature during the spring cruise was more than 10 C lower than that during the autumn cruise. According to the empirical model, the gut evacuation rate constants should have been much higher than in our field results at most stations, especially during the autumn cruise. For example, the gut evacuation rate (0.055 min1) predicted by Dam and Peterson’s empirical model is more than three times higher than that in our in situ measurement at E3 during
Table 6 Community grazing rates of copepods and their grazing pressure on phytoplankton biomass and primary production in the Bohai Sea Primary production (mg C m2 day1)
Community grazing rate
Grazing pressure on
Season
Station
Phytoplankton biomass (mg Chl a m2)
mg C m
% Biomass
Spring
A4 B1 E1 E3
19.2 52.7 31.0 36.8
489.8 237.1 106.0 260.5
9.44 2.29 0.99 1.28
472 115 50 64
37.1 4.3 3.2 3.5
96.4 48.3 46.9 24.7
Autumn
A2 A4 B1 E3
60.1 28.7 31.6 45.9
305.9 78.4 76.3 144.0
1.57 0.57 1.88 4.07
79 28 94 204
2.6 2.0 5.9 8.9
25.7 36.1 122.3 141.4
mg Chl a m
2
2
% Production
C. Li et al. / Estuarine, Coastal and Shelf Science 58 (2003) 487–498
autumn cruise. It is suggested that the negligible effect of temperature on gut evacuation rate constants may be due to the food concentration and composition in this study. The phytoplankton concentration in our study was lower than those employed in the experiments reported by Dam and Peterson. Gut evacuation rate constants of copepod typically decrease at low food concentrations (Dagg & Walser, 1987). Other authors (Dagg, 1993; Small & Ellis, 1992; Zhang et al., 1995) have also reported that their field results were considerably lower than those predicted by the model of Dam and Peterson. 4.2. Ingestion rate and grazing Although the values of GPC of copepod varied widely in this study (see Table 3), they were in the data range reported by others in the same area (Li & Wang, 2000; Wang, Li, Wang, & Zhang, 1998). Other studies have also reported equally large individual variability (Harris, 1996; Uye & Yamamoto, 1995 and others). The values at most stations during the spring cruise were higher than that during the autumn cruise in the study area. This may be due to the higher phytoplankton concentration in spring. Many investigations have shown that zooplankton often exhibit diurnal feeding rhythms with a peak in ingestion during the period of darkness (Dam & Peterson, 1993; Li & Wang, 2000; Wang et al., 1998). However, a few studies have described the diurnal feeding rhythms, where peak values are not reached at night (Durbin, Campbell, Gilman, & Durbin, 1995). Except for the endogenous physiological rhythms, external factors such as food availability and risk of predation have been considered as potential triggering components of copepod diel feeding variation (Bollens, Frost, & Cordell, 1994; Bollens & Stearns, 1992; Huntely & Brooks, 1982). Calbet, Saiz, Irigoien, Alcaraz, and Trepat (1999) reported that copepods (Acartia grani and Centropages typicus) showed clear diel feeding rhythms at high food concentrations, with significantly higher clearance rates during nighttime. When food was limited, however, copepods exhibited different daily feeding pattern, so as to balance the necessity of feeding continuously to obtain the minimum food requirements with the risk of being predated. Some of the results in this study supported this idea. Because the turbidity in an enclosed coastal area is usually higher than that in an open or semi-enclosed area, visual predation may be relatively ineffective (Vinyard & O’Brien, 1976). Thus, copepods living inside the Bohai Bay, with a lower threat of predation, showed relatively small amplitude of feeding rhythms (N/D ratio <1.6). On the other hand, copepods living in the bay-mouth area (stations A2 and A4), where the seawater is relatively clear, should reduce daytime grazing rates to avoid predators. Consequently they presented strong diel feeding rhythms, with the
495
maximal N/D ratio being up to 5.7. Although the mechanism of zooplankton feeding rhythms is complicated and needs further researching, the diel GPC variation of copepods in this study suggests that it is important to measure the GPC during a complete daily cycle when estimating the ingestion rate of zooplankton in the field. The grazing impact of zooplankton on phytoplankton is affected by many factors, including zooplankton abundance and ingestion rate. Many previous studies have shown that the grazing impacts of zooplankton on phytoplankton standing stock and primary production are relatively low. In general, the daily consumption of zooplankton only accounts for <5% of phytoplankton standing stock and <10% of primary production (Barquero et al., 1998; Bautista & Harris, 1992; Dagg, 1995; Li & Wang, 2000; Wang et al., 1998). Higher grazing impact has also been observed in some studies, however. For example, Bathmann, Noji, and Bodungen (1990) reported that the daily grazing of copepod assemblages was equivalent to most of the phytoplankton standing stock and close to or more than primary production during late winter in the Norwegian Sea. The present results showed that grazing by the copepod community was less than 10% of phytoplankton standing stock during both cruises, except at station A4 during spring. This agrees with the previously reported data cited above. The grazing impact on primary production (24.7–96.4% in spring, 25.7–142.8% in autumn) was, however, much higher than cited in some previous reports. The seasonal differences were the result of differences in copepod abundance, feeding rate, phytoplankton biomass and food availability. During the spring cruise, the phytoplankton bloom had developed and the chlorophyll-a concentration was close to the annual maximum in the Bohai Sea. But the copepods need time to numerically respond to the presence of phytoplankton food. According to the historical data, zooplankton biomass increases during spring and reaches its annual maximum in June in the Bohai Sea (Bai & Zhuang, 1991). So, in spring, even though relatively high individual ingestion rates were observed, the community grazing only accounted for small percentage of phytoplankton standing stock. In autumn, the phytoplankton biomass reaches a second peak due to the input of nutrients (Fei, Mao, & Zhu, 1991). Hence, during the autumn cruise, even though the grazing impact on primary production was much higher, such as at stations B1 (142.8%) and E3 (141.4%), the daily consumption was still less than 10% phytoplankton standing stock. Some studies have pointed out that copepods prefer to feed on particles larger than 5–10 lm (Bautista & Harris, 1992; Dam & Peterson, 1991). In this study, size-fractionated chlorophyll-a data showed that, as the average of the observed stations, 82.2 and 78.4% of the phytoplankton biomass during the spring and autumn cruises, respectively, were nanoplankton, i.e. the plankton <5 lm
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(Dr J. Sun, Ocean University of Qingdao, unpublished data). If only the available phytoplankton cells were taken into account, copepods will consume a considerable proportion of the large phytoplankton (>5 lm). Therefore, although the grazing impact of copepods on the phytoplankton standing stock was comparatively lower, it might at the very least have affected the size distribution of the phytoplankton in situ. 4.3. Feeding and the shift of copepod size group Although individual ingestion rates of small-sized animals were lower, they consumed larger amounts of phytoplankton than the other groups during the present study. This was due to the fact that their abundance was very high. These results are similar to that in other studies, which have estimated the relative contribution of size fractions to total copepod community grazing (Barquero et al., 1998; Li & Wang, 2000; Morales et al., 1991; Wang et al., 1998; Zhang et al., 1995). Traditionally, large copepods are thought to have a significant impact by grazing the spring bloom, sometimes suppressing its development. For instance, Calanus finmarchicus have a high grazing impact on spring blooms in the Atlantic when their migration to surface waters occurs as the spring bloom is starting, if the size of their overwintering populations is high enough (Bathmann et al., 1990; Runge, 1988; Tiselius, 1988). The present results support this suggestion at station A4 during the spring cruise. Although the large-sized copepods were few, the medium-sized group (mainly C5 of Calanus sinicus and Centropages mcmurrichi) exhibited a high grazing impact on the phytoplankton standing stock (30.3%) and primary production (59.5%), and they contributed 62% of the total copepod community grazing (Fig. 3). Why then were the small-sized copepods the dominant grazers at other stations in spring and autumn in the Bohai Sea? Based on the data of year-round observations in the Bohai Sea in 1958/1959 and 1992/ 1993, the copepod abundance showed two peaks during the year. Following the spring phytoplankton bloom, the abundance of copepods increased sharply and reached a first peak in June. This peak was mainly due to the arrival and development of a Calanus sinicus population entering the bay from the Yellow Sea and to the rapid growth response of the coastal species (such as Acartia bifilosa, Oithona similis, etc.). In May, C. sinicus mainly distributed in the mouth and central area of the Bohai Sea as well as the local species contributed the major biomass of copepods in the coastal area (Wang et al., 2002). The distribution pattern of copepods during the spring cruise of this study was the same as above. The population of the major large-sized herbivorous copepod, C. sinicus, had developed enough to become the dominant grazer in the mouth of the Bohai Sea
(station A4). However, at the other stations, the local populations, which mainly comprised small-sized species, developed earlier than that of C. sinicus entered with the Yellow Sea waters. Therefore, the small-sized copepods were the dominant grazers at the coastal area (stations B1 and E1). After June, with the water temperature increasing to a high level and phytoplankton concentrations decreasing to a low level, the copepod abundance then decreases to a relatively low level, the large herbivorous copepod C. sinicus decreases dramatically in numbers and finally disappears. Other than the high water temperature (Zhang, Sun, Zhang, & Liu, 2002), limited food availability probably plays an important role in C. sinicus population collapsing. Some studies also suggested that large-sized copepods seem to need higher levels of food for maximal growth and ingestion rates than the co-occurring smaller copepods, and they are probably typically limited by food availability (Harris, 1996; Runge, 1980). The second peak of zooplankton biomass appears in autumn and is mainly due to the continuous development of smallsized copepods, and some large carnivorous species over the summer. Observation over a 2-week period in summer in the Laizhou Bay, located at the south of the Bohai Sea, also indicated the relationship between the food availability and the shift of zooplankton functional groups (Li & Wang, 2000). These conclusions were also supported by theories of food limitation in coastal environments. In coastal food webs, phytoplankton production is generally underexploited by copepod grazing and most of the enhanced phytoplankton production passes through other paths (microbial loop) or sediments to the bottom (Bautista & Harris, 1992). Wang et al. (1998) reported that 35–50% of phytoplankton biomass was consumed by microzooplankton (<200 lm) in the Bohai Sea. In the Bohai Sea, the copepod community apparently consumed only a modest proportion of the standing stock of phytoplankton during spring and autumn blooms, but affected the size distribution of the phytoplankton in situ. They did, however, sometimes graze a significant proportion of daily primary production and hence were presumably able to limit the rate of further accumulation of phytoplankton, or even to prevent it. The smallest-sized copepods (200–500 lm) were most abundant and apparently responsible for most of the grazing, but at the mouth of the Bohai Sea in spring, the population of open sea species (Calanus sinicus and Centropages mcmurrichi) had developed and accounted for 60% of the total community grazing.
Acknowledgements This research was supported by special funds from National Key Basic Research Program of China
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(G19990437) and the National Natural Science Foundation of China (40106016). We thank captain and crew of the R/V Dongfanghong-2 for invaluable assistance in collecting zooplankton samples and in carrying out experiments on board. We are also grateful to Dr Jun Sun for providing the data for primary production and chlorophyll-a and Dr Hao Wei for providing CTD data. Special thanks to D.S. Mchusky and three anonymous reviewers for their valuable comment.
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Grazing impact of copepods on phytoplankton in the Bohai Sea Chaolun Li*, Rong Wang, Song Sun Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, People’s Republic of China Received 2 May 2002; accepted 24 April 2003
Abstract During spring (April/May 1999) and autumn (September/October 1998) cruises in the Bohai Sea, China, copepods were the dominant components of mesozooplankton, the most abundant species being Calanus sinicus, Centropages mcmurrichi, Paracalanus parvus, Acartia bifilosa and Oithona similis. Pigment ingestion rates by three size classes of copepods (200–500, 500–1000 and >1000 lm) were measured. In the south of the investigation area, gut pigment content (GPC), individual pigment-specific ingestion rates and grazing impacts on phytoplankton were lower in spring than in autumn. In the central area, GPC and individual pigmentspecific ingestion rates were higher in spring than in autumn. The grazing impact on phytoplankton by the copepod assemblages was lower in spring than in autumn, however, because of the relatively smaller biomass in spring. In the western area where the Bohai Sea joins the Yellow Sea, GPC, individual pigment-specific ingestion rates and grazing impacts on phytoplankton were higher in spring than in autumn. Among the three size groups, the small-sized animals (200–500 lm) contributed more than 50% (range 38–98%) of the total copepod grazing during both cruises. The grazing impact on phytoplankton by copepods was equivalent to 11.9% (range 3.0– 37.1%) of the chlorophyll-a standing stock and 53.3% (range 21.4–91.4%) of the primary production during the spring cruise. Grazing impact was equivalent to 6.3% (range 2.0–11.6%) of the chlorophyll-a standing stock and >100% (range 25.7–141.6%) of the primary production during the autumn cruise. The copepod community apparently consumed only a modest proportion of the standing stock of phytoplankton during spring and autumn blooms. They did, however, sometimes graze a significant proportion of daily primary production and hence were presumably able to limit the rate of further accumulation of phytoplankton, or even to prevent it. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: copepod; feeding; Bohai Sea
1. Introduction Zooplankton, an integral component of the food web, links phytoplankton production and production of fishes and other animals at higher trophic levels in marine ecosystems. As the GLOBEC Implementation Plan (1999) indicated, ‘‘Reproduction, growth and mortality rates are the essential components of zooplankton population dynamics. The first two of these are under
* Corresponding author. E-mail address: [email protected] (C. Li). 0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(03)00129-X
the direct influence of feeding. Hence studies on feeding of zooplankton are important to advance our understanding of ocean ecosystem dynamics.’’ The emphasis of research on the grazing impact of marine mesozooplankton on phytoplankton has usually been on older stages and larger taxa. Recently, more and more studies have indicated, however, that smaller copepods may often play a more important role than the larger animals not only in terms of abundance, but also in terms of biomass and grazing pressure on the phytoplankton (e.g. Dam & Peterson, 1993; Morales, Bedo, Harris, & Tranter, 1991; Zhang, Dam, White, & Roman, 1995). Studies on feeding in small copepods have been limited, however, because of the diversity of
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Fig. 1. Location of Bohai Sea.
species and developmental stages amongst these smaller taxa. Over the last decade, a body-size approach has been reported as the simplest and most reliable method of dealing with this problem and has been used to estimate the importance of different size fractions in the consumption of phytoplankton (Barquero et al., 1998; Dam, Zhang, Butler, & Roman, 1995; Morales et al., 1991; Williams & Conway, 1988; Zhang et al., 1995). This approach is also appropriate in the sense that this type of ecosystem study should be able to provide order of magnitude estimates as a starting basis for modeling the dynamics within a system (Li & Wang, 2000; Morales et al., 1991). The Bohai Sea is a semi-closed shallow embayment in China with an area of 77,000 km2 (Fig. 1). During the past decades, aquaculture, sea farming and changes in inputs of freshwater, nutrients and sediments have resulted in changes in structure and function of the marine ecosystem. Thus, the Bohai Sea was chosen as one of the China-GLOBEC study areas. One of the components of the project is a study of the feeding of herbivorous copepods in order to improve our understanding of the marine trophic dynamics in this area. This paper presents the seasonal and spatial patterns of size-fractionated copepod grazing in the Bohai Sea, and evaluates the importance of different groups of copepods in terms of their grazing impact on phytoplankton standing stock and primary production.
phytoplankton (Fig. 1). In the autumn cruise, stations A4 and B1 were only occupied for 12 h and E1 was cancelled because of bad weather. Hydrographic conditions and concentrations of chlorophyll-a in each station are shown in Table 1. 2.1. Sampling Zooplankton samples were collected by a net with mouth area of 0.5 m2 and mesh size of 200 lm towed vertically from the bottom to the surface. A flowmeter (T. S. K. made in Japan) was mounted in the center of the mouth of the net to measure the volume of water filtered. Samples were preserved in a 5% formalin– seawater solution. In the laboratory, the entire contents of each sample were sieved through 1000, 500 and 200 lm mesh to divide it into three size fractions. Under a dissecting microscope, 100% of the large, 50–100% of the medium and 10–50% of the small fractions were examined, and the number of copepods was enumerated. Day/night pairs of samples for mesozooplankton abundance were taken at all stations. The mean value of two samples at same station was used to calculate mesozooplankton abundance. Samples for gut pigment analysis and gut evacuation experiments were captured using the same net but with a sealed cod end. 2.2. Gut pigment analysis of zooplankton
2. Materials and methods Two survey cruises were carried out in the Bohai Sea during the spring (April/May 1999) and autumn (October/November 1998). Five stations, where the ship was anchored for 27–30 h, were chosen to study the copepod feeding activities and grazing impact on
Immediately after sampling, the cod-end contents were poured into soda/seawater solution (1 : 5, v/v) to anaesthetize the animals (Kleppel, Frazel, Pieper, & Holliday, 1988), then sieved through 1000, 500 and 200 lm mesh and gently rinsed with filtered seawater to wash away coarse phytoplankton cells. The resultant fractions were sorted under dim light and about 20
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C. Li et al. / Estuarine, Coastal and Shelf Science 58 (2003) 487–498 Table 1 The temperature and chlorophyll-a conditions of survey stations during the study periodsa Temperature ( C)
Chlorophyll-a (mg m3)
Station
Date
Depth (m)
Surface
Bottom
Surface
Bottom
Depth of maximumb
A2
1–2 May 27–28 September 2–3 May 6 October 6–7 May 2–3 October 5–6 May 4–5 May 28–29 September
35
8.8–8.8 22.2–22.7 8.6–9.1 21.7–21.8 11.3–12.1 23.4–23.5 10.3–11.3 8.3–8.8 22.8–23.5
6.7–6.9 20.6–21.8 6.4–6.5 13.9–14.4 11.3–12.0 23.4–23.6 9.8–10.7 7.9–8.1 22.7–22.8
0.22 1.48 0.33 0.44 2.90 2.12 1.39 1.68 1.31
0.98 0.72 0.75 0.35 3.30 1.63 1.83 3.03 0.86
Bottom 10 m (2.03) Bottom 10 m (0.65) Bottom Bottom Bottom Bottom 10 m (1.82)
A4 B1 E1 E3
50 16 19 26
a
Temperatures were measured with a Sea-Bird SBE 9 CTD (H. Wei, personal communication). Chlorophyll-a concentrations were the average values over a daily cycle (J. Sun, personal communication). b The values in the brackets are the concentrations of chlorophyll-a.
animals of the large fraction, 40 of the medium fraction and 80–100 of the small fraction were individually picked and placed in a 10 ml glass centrifuge tube to which 2–3 ml of 90% acetone solution was added. This operation took about 5–10 min. The tube was capped and stored in dark and kept at 30 C. After finishing the whole sampling of one station, the contents of each tube were homogenized in a glass grinder, transferred back to the centrifuge tube, diluted to 10 ml with 90% acetone solution and extracted in dark at 30 C for 24 h. The tubes were then centrifuged for 10 min and the fluorescence of the suspension from each tube was measured before and after acidification with 10% HCl using a Turner Designs model II. Absolute values for chlorophyll-a and phaeopigments were calculated according to Wang and Conover (1986). The sum was used as the index of gut pigment content (GPC). An empirical equation, C ¼ 50chl, was used to convert chlorophyll-a into phytoplankton carbon. 2.3. Diurnal variation in gut pigment content Diurnal variations in GPC were investigated at anchor stations to study the copepod diurnal feeding rhythms. At each station, samples were collected at 3-h intervals for a complete daily cycle and the GPC was measured as above. The night was defined as the time from sunset to sunrise. The amplitude of feeding rhythms of copepods was estimated by the quotient of night/day (N/D) mean GPC. 2.4. Determination of gut evacuation and ingestion rates of copepods Within 5–10 min after capture, living samples for experiments were gently rinsed with filtered seawater to wash away phytoplankton cells and placed in several beakers (2l in number). The beakers contained 0.45 lm filtered seawater to which non-fluorescent charcoal powder (100 lm diameter) was added to keep the
animals under continuous feeding conditions (Willason & Cox, 1987). Beakers were kept in dark submerged in a constant-temperature water bath set to the surface seawater temperature. Initially, and after 10, 20, 30, 60, 90 and 120 min, animals were taken from the respective containers, put into the glass centrifuge tube to which 2–3 ml of 90% acetone solution was added and frozen at 30 C. Subsequent treatments and measurements were the same as the gut pigment analysis. The gut evacuation rate constant (k) was calculated by using a negative exponential equation (Mackas & Bohrer, 1976). Assuming that the animals were feeding at a constant rate, ingestion rates (I) were calculated from the expression I ¼ GPC k where GPC is the average value over a daily cycle. 2.5. Measurements of gut pigment destruction According to Perissinotto and Pakhomov (1996), a two-compartment pigment budget approach was employed to estimate the gut pigment destruction of the copepods at station B1 during the autumn cruise. Freshly collected large-sized copepods (>1000 lm) were allowed to empty their gut pigment for 24 h in filtered seawater with charcoal powder. Several copepods (20– 30 individuals) were then incubated for 30 min in 500 ml bottles filled with natural seawater sampled from 5 m depth. Comparing the decrease in pigment content in the grazing bottles with the increase in GPC of animals incubated in these bottles, any significant loss of the pigments from the experiment treatments was then attributed to gut destruction of the phytoplankton pigments. The gut pigment degradation efficiencies were calculated using the equation b ð%Þ ¼ f1 ½ðGe Pb Þ= Pg100, where Ge is the individual GPC at the end of the incubation, Pb the individual background fluorescence and P is the total amount of individual pigment ingested (Perissinotto & Pakhomov, 1998).
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Table 2 Abundance of potentially herbivorous copepods and dominant species in the Bohai Sea Station
Season
Large (ind. m3)
Species
Medium (ind. m3)
Species
Small (ind. m3)
Species
A2
Spring
107
C. sinicus
408
C. sinicus C. mcmurrichi
1343
Autumn
12
C. sinicus
9
C. teuniremis T. forcipatus
3906
A. bifilosa O. similis C. affinis P. parvus O. similis C. affinis
Spring
46
C. sinicus
3146
5959
Autumn
91
C. sinicus
101
C. C. C. C.
B1
Spring
167
C. sinicus
283
C. sinicus
Autumn
28
C. sinicus
2
C. sinicus
5053
A. bifilosa P. parvus P. parvus
E1
Spring
26
C. sinicus
31
C. sinicus
9022
A. bifilosa
E3
Spring
35
C. sinicus
269
C. sinicus
2483
Autumn
119
C. sinicus
4
T. forcipatu C. teuniremis
10,418
A. bifilosa P. parvus P. parvus O. similis
A4
3. Results 3.1. Zooplankton composition and distribution Concentrations of copepods in the different size fractions and the identities of constituent species are shown in Table 2. Some species occurred in more than one size group because different developmental stages were present. During the spring cruise, the most abundant species in the large-sized group (>1000 lm) was Calanus sinicus. Centropages mcmurrichi represented >72% of the medium-sized group (500–1000 lm). The small-sized group (200–500 lm) was mainly composed of Acartia bifilosa, Paracalanus parvus, Oithona similis and
sinicus mcmurrichi sinicus teuniremis
A. bifilosa O. similis P. parvus O. similis C. affinis
988
23,987
Corycaeus affinis. During the autumn cruise, C. sinicus was also the abundant species in the large-sized group and the same species were present in the small-sized group as those present during the spring cruise. For the medium-sized group, C. mcmurrichi was almost absent, and Centropages teuniremis and Tortanus forcipatus became the dominant species. The small-sized copepods outnumbered the other groups during both cruises.
3.2. Gut pigment contents Results of the copepod GPC are shown in Table 3. Copepod GPC were higher in spring than in autumn
Table 3 The GPC (ng pigm. ind.1) of copepods in the Bohai Sea in 1998/1999 Spring
Autumn
Station
Size
Mean GPC SD
A2
Large Medium Small
No data No data No data
Mean GPC SD
Chl a : Pha
n
2.095 1.822 0.886 0.392 0.565 0.143
0.24 0.27 0.29
9 9 9
A4
Large Medium Small
No data 1.840 1.506 0.485 0.382
0.24 0.23
9 9
1.193 0.303 0.948 0.241 0.438 0.076
0.35 0.31 0.26
5 5 5
B1
Large Medium Small
1.696 0.589 1.132 0.407 0.305 0.138
0.21 0.29 0.21
9 9 9
4.499 2.094 3.172 1.630 1.275 0.175
0.29 0.43 0.34
5 5 5
E1
Large Medium Small
5.500 1.855 1.348 0.806 0.308 0.115
0.16 0.20 0.31
9 9 9
No data No data No data
E3
Large Medium Small
4.619 2.161 2.774 1.370 0.579 0.211
0.21 0.18 0.16
9 9 9
1.424 0.826 0.906 0.345 0.560 0.091
0.23 0.14 0.19
9 9 9
Chl a : Pha
n
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within the middle and mouth stations of the Bohai Sea (stations A4 and E3, Mann–Whitney U-test, p < 0:1). But within the southern station (B1), GPC for all three size groups were higher in autumn than in spring (Mann–Whitney U-test, p < 0:1). During the spring cruise, for large- and medium-sized groups, the maximum of GPC values of copepod was found at station E1 and the lowest values were found at station B1. In spring, small-sized groups had higher values at stations A4 and E3 than at stations E1 and B1 (Mann–Whitney U-test, p < 0:1). During the autumn cruise, the spatial distribution patterns were similar in all three groups. For all size groups, the values of GPC at station B1 were higher than those at other stations (Mann–Whitney U-test, p < 0:1). The diel cycle of GPC of copepods was observed at four stations (A4, B1, E1 and E3) during the spring cruise (Fig. 2a). Diurnal variations in GPC were different amongst size classes and stations. During the spring cruise, both medium- and small-sized animals showed strong diel feeding rhythms at station A4 with peak GPC values at 23:00 hours. The N/D ratios of GPC were 5.7 for the medium-sized and 4.1 for the small-sized copepods. At station B1, for both large- and medium-sized animals, the mean GPC was also higher at night than during the day. There were two high values of gut pigments during a day, however one at 17:00 hours; and the other at 5:00 hours. For the small-sized group, GPC was lower at night and the peak value occurred at 14:00 hours. At station E1, the diel variations of GPC were the same as that at station B1, with higher values for the large- and medium-sized groups and lower values for the small-sized groups at night. The diel feeding patterns of animals at station E3 were similar to those at station A4, but the changes of the GPC were not as large as those at station A4. The N/D ratios of GPC were only 1.3 for large-sized, 1.6 for medium-sized and 1.4 for small-sized copepods. During the autumn cruise, diel variation in GPC was observed only at two stations (A2 and E3). The diel feeding activities of the animals showed the same patterns at both stations. The large- and medium-sized animals fed more actively at night than during the day. The amplitudes of diel feeding rhythms at A2 (N/D ratios were 3.6 for large-sized and 1.6 for medium-sized animals) were higher than those at E3 (N/D ratio was 1.2 for both large- and medium-sized animals). The levels of GPC for the small-sized animals varied insignificantly during a diel cycle, with N/D ratios of about 0.9–1.1.
3.3. Gut evacuation and ingestion rates Eleven gut evacuation experiments were carried out during spring cruise and 12 during autumn cruise (Table 4). Gut evacuation rate constants showed no trend with
491
temperature or body size. The mean gut evacuation rate constant was 0.0174 min1 during the spring cruise and 0.0161 min1 during the autumn cruise. Four culture experiments were carried out to estimate the levels of gut pigment degradation at station B1 during the autumn cruise (Table 5). The gut pigment destruction degree of large-sized copepods was on average 13%, ranging from 0 to 37%. Considering the great differences in water temperatures, chlorophyll-a concentrations, and copepod abundances and compositions, we did not use this result to rectify the ingestion rate, and just used it as a factor to estimate the accuracy of the gut fluorescence method in our study. Daily individual pigment-specific ingestion rates are shown in Table 4. Individual ingestion rates during spring cruise were higher than those measured during autumn cruise for large- and medium-sized groups. The opposite was true for the small-sized animals. Individual ingestion rates at the center (station E3) and mouth (station A4) of the Bohai Sea were higher than those in the coastal area in spring. In autumn, the maximal values were found at station B1.
3.4. Grazing impact Daily grazing rates were calculated from the data on GPC and evacuation rate constants, and then converted to the ratios for the population in the water column from bottom to surface using the population density. The small-sized animals (200–500 lm) were the dominant grazers at most stations during both cruises, except at station B1 during the spring cruise. They contributed more than 60% (range 33.8–88.9%) to the total copepod community grazing during the spring cruise and 80% (range 66.9–97.5%) during the autumn cruise (Fig. 3). The daily grazing rates of the total copepod communities were on average 2.97 mg pigm. m2 day1 (range 0.99–9.44 mg pigm. m2day1) during the spring cruise and 2.10 mg pigm. m2day1 (range 0.57–4.07 mg pigm. m2day1) during the autumn cruise (Table 6). With respect to the in situ phytoplankton biomass, the daily grazing pressure of copepod communities accounted for 11.9% (range 3.2–37.1%) and 5.1% (range 2.0–8.9%) of the total chlorophyll-a standing stocks during spring and autumn cruises, respectively. Assuming a carbon-to-chlorophyll-a ratio of 50, the average carbon-specific grazing rates of copepod communities were calculated as 173 mg C m2day1 (range 50–472 mg C m2day1) during the spring cruise and 105 mg C m2day1 (range 28–204 mg C m2day1) during the autumn cruise (Table 4). The daily consumption of copepod communities was equivalent to an average of 53.3% (range 24.7–96.4%) and 86.5% (range 25.7– 141.4%) of primary production during spring and autumn cruises, respectively.
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Fig. 2. (a) Diurnal variation in GPC of copepods in the Bohai Sea during the spring cruise. (b) Diurnal variation in GPC of copepods in the Bohai Sea during the autumn cruise.
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C. Li et al. / Estuarine, Coastal and Shelf Science 58 (2003) 487–498 Table 4 The results of the experiments to evaluate gut evacuation rate (GER) and individual ingestion rate in the Bohai Sea during the study periods GER (min1)
Individual ingestion rate (ng pigm. ind.1day1)
Season
Station
Temperature ( C)
Large
Medium
Small
Large
Medium
Spring
A4 B1 E1 E3
7.3 11.3 10.3 8.1
No data 0.0250 0.0250 0.0250
0.0203 0.0161 0.0161 0.0154
0.0138 0.0114 0.0114 0.0114
No data 61.1 207.6 259.6
53.8 26.3 31.3 61.4
9.6 5.0 5.0 9.5
176.1 102.9
43.2 17.0
7.3 2.6
91.4 23.5 113.7 30.6
31.1 14.9 72.5 17.2
10.8 7.3 20.6 13.4
33.9 26.7
13.0 2.6
Mean SD Autumn
0.0174 0.0056 A2 A4 B1 E3
22.1 18.7 23.4 22.8
Mean SD
0.0303 0.0139 0.0175 0.0149
0.0244 0.0106 0.0159 0.0132
0.0161 0.0058
4. Discussion 4.1. The gut fluorescence method The gut fluorescence method is currently one of the most available approaches to measure in situ grazing rates of herbivorous zooplankton. One inaccuracy of this method, however, is that pigment destruction occurs during gut passage and that the degree of pigment destruction varies greatly (Cary, Lovette, Perl, Huntley, & Vernet, 1992; Head & Harris, 1992, 1996; Lopez, Huntley, & Sykes, 1988; McLeroy-Etheridge & McManus, 1999; Penry & Frost, 1991; Stevens & Head, 1998; Wang & Conover, 1986). In the present study, culture experiments at station B1 were conducted to estimate the gut pigment destruction degree of large-sized copepods in the autumn cruise. The results showed that the pigment loss ranged from no degradation to 37% (13% on average; Table 5), which was in the data range reported in some previous results obtained in situ or in the laboratory (Head & Harris, 1996; Landry, Lorenzen, & Peterson, 1994; Landry, Peterson, & Fagerness, 1994; Penry & Frost, 1991). The degree of pigment destruction was related to several factors, including ingestion rate, zooplankton behavior, ambient conditions and the prior feeding history (Head & Harris, 1992, 1996; Penry & Frost, 1991; Stevens & Head, 1998; Tirelli & Mayzaud, 1998). Instead of being starved in the filtered seawater, copepods were fed only charcoal particles for 24 h to clear their guts of fluorescence before the culture
0.0133 0.0116 0.0112 0.0167
64.8 44.6
Small
experiments in this study. This should keep the filterfeeder copepods under active feeding conditions, with particle ingestion and faecal egestion proceeding uninterruptedly (Perissinotto & Pakhomov, 1996; Willason & Cox, 1987). Thereby, it is possible that the present results represented a situation much closer to in situ conditions. Because the concentrations of chlorophylla and copepod ingestion rates were greatly different amongst the stations, it was improper to use the results of station B1 to rectify the ingestion rates of all stations. However, the average value of GPC degradation rates of station B1 (13%) agreed with the idea in Harris’ (1996) review that pigment destruction rates are low (<20%) in the chlorophyll range that most animals will experience in nature, so high pigment loss may not be such a significant factor in the natural environment. Therefore, it is suggested that our measurements of GPC were not underestimated by more than 20%. This underestimation would not change the general conclusions of this paper. Another possible inaccuracy of the gut fluorescence method is associated with the determination of the gut evacuation rate constant. Several factors may affect the results of the gut evacuation experiments, such as the temperature, initial gut content, duration of experiment, incubation in filtered seawater and the intrinsic feeding rhythms (Dam & Peterson, 1988; Head, 1988; Tirelli & Mayzand, 1998; Wang & Conover, 1986). In this investigation, the individuals for gut evacuation experiment were incubated in the filtered seawater with charcoal powder (100 lm diameter) added to keep
Table 5 Estimation of pigment destruction efficiency for large copepods at Station B1 during the autumn cruise Experiment number
Chlorophyll-a concentration (mg m3)
Pigment ingested (ng pigm. ind1)
Pigment recovered (ng pigm. ind.1)
Destruction efficiency (%)
1 2 3 4
1.97 3.94 1.76 2.23
5.58 0.83 6.61 0.92 7.65 4.93 2.34 0.33
5.27 0.91 6.72 1.12 4.85 3.95 1.92 0.42
5.5 3.5 0a 36.5 12.6 18.8 6.4
a
Considering the limits of error, the pigment destruction efficiency in experiment 2 is 0%.
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Fig. 3. Percentage contribution to the total grazing by 200–500, 500–1000 and >1000 lm copepods.
the animals under continuous feeding conditions, and the experiments lasted for 90–120 min, attempting to represent a situation closer to in situ condition. The results confirmed that the gut evacuation rate constants were independent of body size, which has been verified in previous studies (Morale, Bautista, & Harris, 1990; Zhang et al., 1995). Temperature was considered to have the dominant influence on gut evacuation rate constant and an empirical model has been proposed to define their relationship (Dam & Peterson, 1988). Field results showed no relationship between the temperature and
the gut evacuation rate in our study, however. There was no obvious difference between the two seasons, even though the seawater temperature during the spring cruise was more than 10 C lower than that during the autumn cruise. According to the empirical model, the gut evacuation rate constants should have been much higher than in our field results at most stations, especially during the autumn cruise. For example, the gut evacuation rate (0.055 min1) predicted by Dam and Peterson’s empirical model is more than three times higher than that in our in situ measurement at E3 during
Table 6 Community grazing rates of copepods and their grazing pressure on phytoplankton biomass and primary production in the Bohai Sea Primary production (mg C m2 day1)
Community grazing rate
Grazing pressure on
Season
Station
Phytoplankton biomass (mg Chl a m2)
mg C m
% Biomass
Spring
A4 B1 E1 E3
19.2 52.7 31.0 36.8
489.8 237.1 106.0 260.5
9.44 2.29 0.99 1.28
472 115 50 64
37.1 4.3 3.2 3.5
96.4 48.3 46.9 24.7
Autumn
A2 A4 B1 E3
60.1 28.7 31.6 45.9
305.9 78.4 76.3 144.0
1.57 0.57 1.88 4.07
79 28 94 204
2.6 2.0 5.9 8.9
25.7 36.1 122.3 141.4
mg Chl a m
2
2
% Production
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autumn cruise. It is suggested that the negligible effect of temperature on gut evacuation rate constants may be due to the food concentration and composition in this study. The phytoplankton concentration in our study was lower than those employed in the experiments reported by Dam and Peterson. Gut evacuation rate constants of copepod typically decrease at low food concentrations (Dagg & Walser, 1987). Other authors (Dagg, 1993; Small & Ellis, 1992; Zhang et al., 1995) have also reported that their field results were considerably lower than those predicted by the model of Dam and Peterson. 4.2. Ingestion rate and grazing Although the values of GPC of copepod varied widely in this study (see Table 3), they were in the data range reported by others in the same area (Li & Wang, 2000; Wang, Li, Wang, & Zhang, 1998). Other studies have also reported equally large individual variability (Harris, 1996; Uye & Yamamoto, 1995 and others). The values at most stations during the spring cruise were higher than that during the autumn cruise in the study area. This may be due to the higher phytoplankton concentration in spring. Many investigations have shown that zooplankton often exhibit diurnal feeding rhythms with a peak in ingestion during the period of darkness (Dam & Peterson, 1993; Li & Wang, 2000; Wang et al., 1998). However, a few studies have described the diurnal feeding rhythms, where peak values are not reached at night (Durbin, Campbell, Gilman, & Durbin, 1995). Except for the endogenous physiological rhythms, external factors such as food availability and risk of predation have been considered as potential triggering components of copepod diel feeding variation (Bollens, Frost, & Cordell, 1994; Bollens & Stearns, 1992; Huntely & Brooks, 1982). Calbet, Saiz, Irigoien, Alcaraz, and Trepat (1999) reported that copepods (Acartia grani and Centropages typicus) showed clear diel feeding rhythms at high food concentrations, with significantly higher clearance rates during nighttime. When food was limited, however, copepods exhibited different daily feeding pattern, so as to balance the necessity of feeding continuously to obtain the minimum food requirements with the risk of being predated. Some of the results in this study supported this idea. Because the turbidity in an enclosed coastal area is usually higher than that in an open or semi-enclosed area, visual predation may be relatively ineffective (Vinyard & O’Brien, 1976). Thus, copepods living inside the Bohai Bay, with a lower threat of predation, showed relatively small amplitude of feeding rhythms (N/D ratio <1.6). On the other hand, copepods living in the bay-mouth area (stations A2 and A4), where the seawater is relatively clear, should reduce daytime grazing rates to avoid predators. Consequently they presented strong diel feeding rhythms, with the
495
maximal N/D ratio being up to 5.7. Although the mechanism of zooplankton feeding rhythms is complicated and needs further researching, the diel GPC variation of copepods in this study suggests that it is important to measure the GPC during a complete daily cycle when estimating the ingestion rate of zooplankton in the field. The grazing impact of zooplankton on phytoplankton is affected by many factors, including zooplankton abundance and ingestion rate. Many previous studies have shown that the grazing impacts of zooplankton on phytoplankton standing stock and primary production are relatively low. In general, the daily consumption of zooplankton only accounts for <5% of phytoplankton standing stock and <10% of primary production (Barquero et al., 1998; Bautista & Harris, 1992; Dagg, 1995; Li & Wang, 2000; Wang et al., 1998). Higher grazing impact has also been observed in some studies, however. For example, Bathmann, Noji, and Bodungen (1990) reported that the daily grazing of copepod assemblages was equivalent to most of the phytoplankton standing stock and close to or more than primary production during late winter in the Norwegian Sea. The present results showed that grazing by the copepod community was less than 10% of phytoplankton standing stock during both cruises, except at station A4 during spring. This agrees with the previously reported data cited above. The grazing impact on primary production (24.7–96.4% in spring, 25.7–142.8% in autumn) was, however, much higher than cited in some previous reports. The seasonal differences were the result of differences in copepod abundance, feeding rate, phytoplankton biomass and food availability. During the spring cruise, the phytoplankton bloom had developed and the chlorophyll-a concentration was close to the annual maximum in the Bohai Sea. But the copepods need time to numerically respond to the presence of phytoplankton food. According to the historical data, zooplankton biomass increases during spring and reaches its annual maximum in June in the Bohai Sea (Bai & Zhuang, 1991). So, in spring, even though relatively high individual ingestion rates were observed, the community grazing only accounted for small percentage of phytoplankton standing stock. In autumn, the phytoplankton biomass reaches a second peak due to the input of nutrients (Fei, Mao, & Zhu, 1991). Hence, during the autumn cruise, even though the grazing impact on primary production was much higher, such as at stations B1 (142.8%) and E3 (141.4%), the daily consumption was still less than 10% phytoplankton standing stock. Some studies have pointed out that copepods prefer to feed on particles larger than 5–10 lm (Bautista & Harris, 1992; Dam & Peterson, 1991). In this study, size-fractionated chlorophyll-a data showed that, as the average of the observed stations, 82.2 and 78.4% of the phytoplankton biomass during the spring and autumn cruises, respectively, were nanoplankton, i.e. the plankton <5 lm
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(Dr J. Sun, Ocean University of Qingdao, unpublished data). If only the available phytoplankton cells were taken into account, copepods will consume a considerable proportion of the large phytoplankton (>5 lm). Therefore, although the grazing impact of copepods on the phytoplankton standing stock was comparatively lower, it might at the very least have affected the size distribution of the phytoplankton in situ. 4.3. Feeding and the shift of copepod size group Although individual ingestion rates of small-sized animals were lower, they consumed larger amounts of phytoplankton than the other groups during the present study. This was due to the fact that their abundance was very high. These results are similar to that in other studies, which have estimated the relative contribution of size fractions to total copepod community grazing (Barquero et al., 1998; Li & Wang, 2000; Morales et al., 1991; Wang et al., 1998; Zhang et al., 1995). Traditionally, large copepods are thought to have a significant impact by grazing the spring bloom, sometimes suppressing its development. For instance, Calanus finmarchicus have a high grazing impact on spring blooms in the Atlantic when their migration to surface waters occurs as the spring bloom is starting, if the size of their overwintering populations is high enough (Bathmann et al., 1990; Runge, 1988; Tiselius, 1988). The present results support this suggestion at station A4 during the spring cruise. Although the large-sized copepods were few, the medium-sized group (mainly C5 of Calanus sinicus and Centropages mcmurrichi) exhibited a high grazing impact on the phytoplankton standing stock (30.3%) and primary production (59.5%), and they contributed 62% of the total copepod community grazing (Fig. 3). Why then were the small-sized copepods the dominant grazers at other stations in spring and autumn in the Bohai Sea? Based on the data of year-round observations in the Bohai Sea in 1958/1959 and 1992/ 1993, the copepod abundance showed two peaks during the year. Following the spring phytoplankton bloom, the abundance of copepods increased sharply and reached a first peak in June. This peak was mainly due to the arrival and development of a Calanus sinicus population entering the bay from the Yellow Sea and to the rapid growth response of the coastal species (such as Acartia bifilosa, Oithona similis, etc.). In May, C. sinicus mainly distributed in the mouth and central area of the Bohai Sea as well as the local species contributed the major biomass of copepods in the coastal area (Wang et al., 2002). The distribution pattern of copepods during the spring cruise of this study was the same as above. The population of the major large-sized herbivorous copepod, C. sinicus, had developed enough to become the dominant grazer in the mouth of the Bohai Sea
(station A4). However, at the other stations, the local populations, which mainly comprised small-sized species, developed earlier than that of C. sinicus entered with the Yellow Sea waters. Therefore, the small-sized copepods were the dominant grazers at the coastal area (stations B1 and E1). After June, with the water temperature increasing to a high level and phytoplankton concentrations decreasing to a low level, the copepod abundance then decreases to a relatively low level, the large herbivorous copepod C. sinicus decreases dramatically in numbers and finally disappears. Other than the high water temperature (Zhang, Sun, Zhang, & Liu, 2002), limited food availability probably plays an important role in C. sinicus population collapsing. Some studies also suggested that large-sized copepods seem to need higher levels of food for maximal growth and ingestion rates than the co-occurring smaller copepods, and they are probably typically limited by food availability (Harris, 1996; Runge, 1980). The second peak of zooplankton biomass appears in autumn and is mainly due to the continuous development of smallsized copepods, and some large carnivorous species over the summer. Observation over a 2-week period in summer in the Laizhou Bay, located at the south of the Bohai Sea, also indicated the relationship between the food availability and the shift of zooplankton functional groups (Li & Wang, 2000). These conclusions were also supported by theories of food limitation in coastal environments. In coastal food webs, phytoplankton production is generally underexploited by copepod grazing and most of the enhanced phytoplankton production passes through other paths (microbial loop) or sediments to the bottom (Bautista & Harris, 1992). Wang et al. (1998) reported that 35–50% of phytoplankton biomass was consumed by microzooplankton (<200 lm) in the Bohai Sea. In the Bohai Sea, the copepod community apparently consumed only a modest proportion of the standing stock of phytoplankton during spring and autumn blooms, but affected the size distribution of the phytoplankton in situ. They did, however, sometimes graze a significant proportion of daily primary production and hence were presumably able to limit the rate of further accumulation of phytoplankton, or even to prevent it. The smallest-sized copepods (200–500 lm) were most abundant and apparently responsible for most of the grazing, but at the mouth of the Bohai Sea in spring, the population of open sea species (Calanus sinicus and Centropages mcmurrichi) had developed and accounted for 60% of the total community grazing.
Acknowledgements This research was supported by special funds from National Key Basic Research Program of China
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(G19990437) and the National Natural Science Foundation of China (40106016). We thank captain and crew of the R/V Dongfanghong-2 for invaluable assistance in collecting zooplankton samples and in carrying out experiments on board. We are also grateful to Dr Jun Sun for providing the data for primary production and chlorophyll-a and Dr Hao Wei for providing CTD data. Special thanks to D.S. Mchusky and three anonymous reviewers for their valuable comment.
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