Aquatic Ecology 38: 485–493, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands.
485
The dynamics of microbial and herbivorous food webs in a coastal sea with special reference to intermittent nutrient supply from bottom intrusion Shin-ichi Nakano1,2,*, Yuji Tomaru3,4, Toshiya Katano1, Atsushi Kaneda1, Wataru Makino1,5, Yuichiro Nishibe3,6, Miho Hirose3,7, Masashi Onji1,8, Shin-Ichi Kitamura1,9 and Hidetaka Takeoka1 1Center
for Marine Environmental Studies, Ehime University, Bunkyo-cho 3, Matsuyama 790-8577, Ehime, Japan; 2Current address: Laboratory of Aquatic Food Web Dynamics, Faculty of Agriculture, Ehime University, Tarumi 3-5-7, Matsuyama 790-8566, Ehime, Japan; 3Faculty of Agriculture, Ehime University, Tarumi 3-5-7, Matsuyama 790-8566, Ehime, Japan; 4Current address: National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, Maruishi 2-17-5, Ohno-cho, Saeki-gun 739-0452, Hiroshima, Japan; 5Current address: Graduate School of Life Science, Tohoku University, Aramaki Aza Aoba, Sendai, Miyagi 980-8578, Japan; 6Current address: Graduate School of Fisheries Science, Hokkaido University, 3-1-1 Minatocho, Hakodate 041-8611, Hokkaido, Japan; 7Current address: Nippon Becton Dickinson Company, Ltd., Akasaka DS Building, 5-26, Akasaka 8-Chome, Minatoku, Tokyo, 107, Japan; 8Current address: Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Fukuoka, Japan; 9Current address: Department of Aqualife Medicine, Yosu National University, San 96-1 Dunduk-dong Yeosu, Jeollanam-do, 550-749 Korea; *Author for correspondence (e-mail:
[email protected]) Received 24 November 2003; Accepted in revised form 24 May 2004
Key words: Autotrophic picoplankton, Bacteria, Diatoms, Flagellates, Nutrients, Physical event
Abstract Seasonal changes in abundance of planktonic microorganisms, together with some physico-chemical variables, were monitored monthly from May 1999 to March 2002 in the surface water of a coastal bay where nutrients are mainly supplied by intermittent intrusions of deeper water 共bottom intrusion兲. No significant bottom intrusion was detected in 1999 but large or frequent bottom intrusions were found from June to October in 2000, and again from mid-June only to late July in 2001. These results indicate that there is a different nutrient supply every year, and peaks in the abundance of dominant eukaryotic phytoplankton 共diatoms and dinoflagellates兲 roughly corresponded to the occurrences of bottom intrusions. By contrast, there was a cyclic seasonal pattern of autotrophic picoplankton 共APP兲 cell density, which reached maxima in August of every year at very similar levels 共4.0-5.0 ⫻ 105 cells ml–1兲. Thus, the seasonal abundance of APP was apparently independent of the occurrence of bottom intrusions. Seasonal changes in cell densities of heterotrophic bacteria showed similar trends to the APP, and temperature-dependent growth of both was indicated. The present study suggests that the matter cycling in the bay varies as a result of shifts in the dominant food linkages, from a microbial food web to a herbivorous food web, due to intermittent nutrient supplies from bottom intrusions.
486 Introduction In marine environments, the dominant phytoplankton change as eutrophication proceeds. For example, autotrophic picoplankton 共APP兲 dominate in oligotrophic waters, while colonial cyanobacteria or eukaryotic algae dominate in more eutrophic systems 共Agawin et al. 2000; Duarte et al. 2000; Bell and Kalff 2001; Crosbie and Furnas 2001兲. It is well known that APP such as Synechococcus and Prochlorococcus play important roles in microbial food webs, whereas nanoplankton and micro-sized phytoplankton such as diatoms and phytoflagellates do so in herbivorous food webs 共Stockner and Antia 1986; Weisse 1993兲. Thus, along a gradient leading to eutrophy, the relative importance of the food supply in the cycling of matter within an aquatic system will shift from dominance by a microbial food web to dominance of a herbivorous food web. The importance of these two food sources for metazoan zooplankton has been examined in artificially enclosed waters in order to maintain stable conditions 共Ducklow et al. 1986; Koshikawa et al. 1996兲. However, controversy continues over the relative importance of the microbial food web and the herbivorous food web as the major source of organic matter input to metazoan zooplankton 共Sherr et al. 1987; Legendre and Rassoulzadegan 1995兲. In contrast, in some seas in which nutrient inputs occur from intermittent events such as upwelling and intrusion 共Walsh et al. 1974, 1978兲, the trophic states of these waters change from oligotrophic to meso- or eutrophic state. Hence, the role of the two food types
in the cycling of organic matter may also shift following changes in trophic status. Painting et al. 共1993a, 1993b兲 have investigated temporal changes in the biomass relationships and community structure of the planktonic food web during the development of a plume of upwelled water in the southern Benguela upwelling region. They simulated using a theoretical size-based model and noted that mesozooplankton would consume the diatoms if abundant but after the senescence of a diatom bloom will feed on the microzooplankton that feed on APP and heterotrophic bacteria. Unfortunately, our knowledge about shifts of dominant food linkages in an aquatic system in relation to changes in its trophic state is limited. The Uwa Sea is the coastal area of Shikoku Island, Japan 共Figure 1兲 where cultivation of the pearl oyster Pinctada fucata is the most productive in Japan. The larvae of the oyster graze picoplankton including heterotrophic bacteria and APP 共Tomaru et al. 2000兲. Studies on the ecology of the microbial food web in this area are important, not only for theoretical view points of food web structure and function, but also from view point of fisheries management. There are two major physical events in the Uwa Sea: kyucho and bottom intrusion. The former is an intrusion of surface, warm and oligotrophic water from the south of the Bungo Channel to the west coast of Shikoku Island, which occurs mainly in summer 共Takeoka and Yoshimura 1988; Takeoka et al. 1993兲. Bottom intrusion consists of deep, cold and nutrient-rich water that flows just over the continental shelf 共Takeoka et al. 2000; Kaneda et al. 2002 a, b兲, serving as the major nutrient source to the coastal areas 共Koizumi 1991;
Figure 1. Map of Uchiumi Bay, Japan showing the sampling station 共Ub兲 and thermistor station 共Ut兲.
487 Koizumi and Kohno 1994; Koizumi et al. 1997; Takeoka et al. 2000; Kaneda et al. 2002 a, b兲. While the effect of kyucho on phytoplankton growth is negligible, diatom blooms promoted by nutrient inputs from bottom intrusion have been observed in a bay of the Uwa Sea 共Koizumi and Kohno 1994; Koizumi et al. 1997兲. Thus, the trophic status of the area is temporarily changed during such bottom intrusions. Studies of a coastal area of the Uwa Sea could therefore provide useful information about shifts in the relative importance of the two food linkages in matter cycling of the system following changes in its trophic state. In the surface water of a bay in the Uwa Sea we followed the temporal changes in the structure of the planktonic food web due to bottom intrusions to examine the hypothesis that shifts of dominant food linkages occur in relation to changes in its trophic state. The abundance of planktonic microorganisms was monitored, together with some physico-chemical parameters.
Materials and methods The study was carried out in Uchiumi Bay located in Iegushi, Uchiumi Village, Ehime Prefecture, Japan 共Figure 1兲. The information about depth, water movements, stratification condition of the bay is available in Takeoka et al. 共1997兲. There are no rivers or streams flowing into the bay, so there is negligible effect on water quality by nutrient loading of inflows. The bay is oligo- to mesotrophic, judging from its chlorophyll level of usually ⬍ 2 g l–1 共Tomaru et al. 2002兲. Thermal stratification in the bay usually develops from May to October of the year. Water temperatures in the bay were measured at 2 and 60 m depths, every 30 minutes using a thermistor chain 共station Ut, depth ca. 61 m兲 共Figure 1兲, since 1996 by the Ehime Prefectural Fishermen’s Cooperative Association 共Kaneda et al. 2002 a, b兲, who allowed us to use their data. The sampling station 共Ub, depth ca. 53 m兲 was located at the center of the pearl oyster culture farm 共Figure 1兲. Water samples were collected monthly from 2-m depth using a 6L Van-Dorn water sampler. The samples for enumeration of plankton were collected from May 1999 to March 2002, and those for determining concentrations of soulble reactive phosphorus 共SRP兲 from May 2000 to March 2001. A 100 ml aliquot of the water sample was filtered through a
0.2 m filter 共Nuclepore兲, and the filtrate used for determination of SRP by the method of Murphy and Riley 共1962兲. Immediately after sampling, another 100 ml portion was fixed with glutaraldehyde at a final concentration of 1% for enumeration of autotrophic picoplankton 共APP兲, heterotrophic bacteria and nanoflagellates which are potential picoplankton consumers 共Azam et al. 1983; Stockner and Antia 1986; Dolan and Simek 1998, 1999兲. We used 20–50 ml of the fixed water sample for enumeration of APP, 1-2 ml for heterotrophic bacteria and 30–50 ml for counting flagellates. After filtering the fixed water sample through a black-stained 0.2 m Nuclepore filter, APP was enumerated by autofluorescence using an epifluorescence microscope under green excitation light. Most APP cells enumerated probably belonged to the genus Synechococcus. Heterotrophic bacteria and nanoflagellates were also counted using the epifluorescence microscope under ultraviolet excitation by the DAPI 共Porter and Feig 1980兲 and primulin 共Caron 1983兲 methods, using black-stained 0.2 and 0.8 m Nuclepore filters, respectively. We could not discriminate flagellates into autotrophic and heterotrophic ones due to weak autofluorescence under an epifluorescence microscope. Hence, cells ⬍ 20 m with flagella were counted as nanoflagellates. At least 100 APP cells, 300 cells of heterotrophic bacteria and 30 nanoflagellate cells were counted at least twice in each sample: the CVs of these counts were 5.0 %, 3.8 % and 10 %, respectively. For enumeration of nano- and microphytoplankton, another 500 ml of the sample was fixed with acidified Lugol’s solution to a final concentration of 1%. Phytoplankton cells were identified to genus and counted using a haematocytometer under a microscope at ⫻ 200 or ⫻ 400 magnification.
Results The surface water temperatures ranged annually between 16.0 and 26.0 °C in 1999, 14.3 and 28.0 °C in 2000 and 15.5 and 29.0 °C in 2001 共Figure 2兲. The surface water temperature 共2 m兲 showed a similar seasonal pattern in each year, although there are gaps in the data, especially for the summer of 1999 共Figure 2兲. In contrast, the seasonal pattern of bottom temperature 共60 m兲 differed annually 共Figure 2兲. In 1999, the bottom temperature also increased with that
488 in the surface from April to August 共Figure 2兲, but in 2000, the bottom water temperature did not markedly increase, until mid October 共Figure 2兲. In 2001, the bottom water temperature co-varied with surface water temperature between January and early June, decreased from mid-June to late July, and increased from August to early October 共Figure 2兲. The SRP concentration at 2 m ranged between below the detection limit 共May 2001兲 and 4.4 mol P l–1 共October 2000兲 共Figure 3兲. It increased substantially from September to October 2000, remained high from October to January 2001, decreased remarkably from February 2001 to May 2001, remained low until October 2001 and slightly increased from November 2001 onwards. There was a cyclic seasonal pattern of autotrophic picoplankton 共APP兲 cell densities at 2 m 共Figure 4A兲 with similar annual maxia in August: 5.0 ⫻ 105 cells ml–1 in 1999, 4.7 ⫻ 105 cells ml–1 in 2000 and 4.0 ⫻ 105 cells ml–1 in 2001. The dominant phytoplankton groups at 2 m were diatoms and dinoflagellates 共Figure 4B, Figure 4C兲. Diatoms, predominantly Nitzschia and Chaetoceros, usually had blooms from April to June 共Figure 4B兲, but they were more abundant in 2000 than in 1999 and 2001 共Figure 4B兲. The densities of dinoflagellates remained low in 1999, but higher densities were detected in 2000 and 2001 with the maxima of 200 cells ml–1 in August 2000 and 99 cells ml–1 in May 2001, respectively 共Figure 4C兲. Dominant dinoflagellate taxa in 2000 and 2001 were Gymnodinium and Protoperidinium. Cyclic seasonal patterns were also found in the bacterial cell densities at 2 m 共Figure 5A兲. The maximal densities in 1999 共4.2 ⫻ 106 cells ml–1兲 and 2000 共3.7 ⫻ 106 cells ml–1兲 were detected in August, although their maximum in 2001 was measured in June 共2.5 ⫻ 106 cells ml–1兲 共Figure 5A兲. By contrast, cell density of nanoflagellates fluctuated irregularly during the study period 共Figure 5B兲.
Discussion
Figure 2. Changes in water temperatures at depths of 2 m and 60 m in Uchiumi Bay, from 1999 to 2001.
Among the physical events in the ocean, upwelling is one of the well-known events that cold subsurface water rises to the surface. Upwellings are found in the Californian coast, the Peruvian coast, the Senegal coast and so on, caused by wind effects 共Beer 1983兲. In contrast, bottom intrusion detected in the present study is caused due to the spring-neap tidal modulation 共Kaneda et al. 2002兲. Thus, the generation
489
Figure 3. Changes in concentration of soluble reactive phosphorus 共SRP兲 at 2 m depth in Uchiumi Bay from May 2000 to March 2002.
mechanism of the bottom intrusion is essentially different from that of upwelling. Cold, bottom water that intrudes into Uchiumi Bay is rich in nutrients 共Takeoka et al. 2000兲. It causes a decrease of temperature in the deeper layers and increase in temperature heterogeneity between surface and bottom temperature 共Kaneda et al. 2002 a, b兲. In 1999, the temperature difference was relatively small 共Figure 2A兲, indicating that bottom intrusion was absent or low. In contrast, in 2000 temperatures at 2m and 60 m differed considerably from June to mid October 共Figure 2B兲, indicating either large or frequent bottom intrusions. In 2001, bottom intrusions were detected only from mid-June to late July 共Figure 2C兲. Takeoka et al. 共1997兲 estimated the fraction of the available vertical mixing energy in the loss of tidal kinetic energy due to bottom friction 共⑀兲 in Uchiumi Bay. The ⑀ of Uchiumi Bay 共1.4兲 was much higher than those estimated for other waters: 0.015 for Bungo channel 共Yanagi and Ohba 1985兲, and 0.0028 for the Irish Sea 共Simpson and Hunter 1974兲. This suggests that Uchiumi Bay is susceptible to vertical mixing and that nutrients transported to the bay by bottom intrusions are likely to reach the surface water by vertical mixing. High SRP concentrations 共Figure 3兲 were detected in the bay between October 2000 and January 2001 共Figure 2B兲, whereas the concentrations from February 2001 onwards were relatively low 共Figure 3兲. Since a large bottom intrusion was detected from early to mid October 2000 共Figure 2兲, the high SRP concentration in this period was attributable to nutrients supplied by the bottom intrusion. Vertical mixing due to autumnal wind action in the
water column between mid October 2000 and January 2001 共Figure 2兲 may also cause high SRP values due to transport of SRP from the deeper to the surface layers. Despite the large or frequent bottom intrusions in 2000, SRP concentrations from mid-June to September 2000 were low 共Figure 3兲, and this is likely to be due to utilization of nutrients by phytoplankton. Indeed, we had a red tide of dinoflagellates between July and August in 2000 共Figure 4C兲. High phytoplankton abundance, probably stimulated by nutrient supply through bottom intrusion, was also detected in June 2001, although we cannot explain the high abundance of phytoplankton found in May 2001. Studies in the Uwa Sea have demonstrated that nutrients supplied by bottom intrusions caused massive growth of diatoms 共Koizumi and Kohno, 1994; Koizumi et al., 1997兲, and it is well known that nutrient supply by upwelling causes algal blooms 共Houghton and Mensah 1978; Walsh et al. 1978; Yoder et al. 1981; Painting et al. 1993a兲. Thus, we have demonstrated the enhancement of phytoplankton growth by nutrients supplied through bottom intrusion, which is a different physical event from upwelling. Unlike diatoms and dinoflagellates, the seasonal pattern of changes in APP abundance did not follow the occurrence of bottom intrusion 共Figure 4A 兲. In addition, the annual maxima for APP were similar 共Figure 4A兲, although the occurrence and extent of bottom intrusion annually varied 共Figure 2兲. Thus, the seasonal abundance of APP is independent of the nutrients supplied by bottom intrusion. Hall and Vincent 共1990兲 reported that nutrient supplies in a west coast
490
Figure 4. Changes in cell densities of 共A兲 autotrophic picoplankton 共APP兲, 共B兲 diatoms and 共C兲 dinoflagellates at 2 m depth in Uchiumi Bay from May 1999 to March 2002.
upwelling-area off the South Island of New Zealand did not favor dominance by Synechococcus, as was simulated by the ecological model of Kumar et al. 共1994兲. The results of the present study, in which the responses of APP to the nutrient supply was negligible and larger phytoplankton was positive, support the results of Hall and Vincent 共1990兲. On the Great Barrier Reef, growth rates of Synechococcus and Prochlorococcus were saturated at low dissolved inorganic nitrogen 共DIN兲 concentrations, whereas those of diatoms were related to DIN concentration 共Crosbie and Furnas, 2001兲. In mesocosm experiments conducted in the Mediterranean Blanes Bay,
Duarte et al. 共2000兲 found that APP dominated by Synechococcus grew in response to increased nutrient inputs but this growth rate was much lower than that of microphytoplankton which subsequently increased in abundance. Thus, it is suggested that the negligible response of APP to increase in nutrient concentration due to supplied by bottom intrusion in the present study was due to saturation of the APP growth rate already under the ambient nutrient levels. Moreover, it has also been suggested that in oligotrophic environments APP are superior competitors for uptake of nutrients at low levels, probably due to their high surface-to-volume 共S/V兲 ratios 共Smith and Kalff
491
Figure 5. Changes in cell densities of 共A兲 heterotrophic bacteria and 共B兲 nanoflagellates at 2 m depth in Uchiumi Bay from May 1999 to March 2002.
1982; Weisse 1993兲. These may be the reasons why the seasonal abundance of APP was apparently independent of the occurrence of bottom intrusion. The seasonal pattern of densities of heterotrophic bacteria 共Figure 5A兲 was similar to that of APP 共Figure 4A兲. Heterotrophic bacteria in natural aquatic environments also have high cellular S/V ratios 共Kirchman, 1994兲, and are superior competitors for uptake of nutrients at low concentrations 共Currie and Kalff ,1984 a, b, c; Kirchman, 1994兲. Thus, the abundance of heterotrophic bacteria as that of APP in Uchiumi Bay may be subjected to environmental regulation. APP densities were also relatively high in May and June 共Figure 4A兲, which is when thermal stratification starts in Uchiumi Bay. Seasonal abundance of APP in the bay may depend on water temperature, and this is also plausible for that of heterotrophic bacteria. Similar results were also noted by El Hag and Fogg 共1986兲 and Pitcher et al. 共1991兲. Watson and MacCauley 共1988兲 reported that the growth rates of edible, small phytoplankton such as pico- and nanophytoplankton were potentially enhanced by high nutrient levels in eutrophic waters although their biomasses were strongly depressed by
heavy grazing. Thus, grazing by protists and/or other microzooplankton may be an important loss process for APP during the occurrence of bottom intrusion. Using cross system analysis, Sanders et al. 共1992兲 reported that abundance of heterotrophic bacteria in eutrophic systems is mainly controlled by grazing, while that in oligotrophic systems it is controlled by supply of dissolved organic matter derived from phytoplankton. Since Uchiumi Bay, if only temporarily, becomes more eutrophic when bottom intrusion occurs, grazing may also be of major importance for controlling the abundance of heterotrophic bacteria in the bay during that period. The most important potential grazers of APP and heterotrophic bacteria in marine environments are heterotrophic nanoflagellates 共Azam et al. 1983; Stockner and Antia 1986; Dolan and Simek 1998, 1999兲 but their seasonal abundance differed from that of APP and heterotrophic bacteria, although they did became relatively abundant in August 共Figure 5B兲. We regard not only heterotrophic but also autotrophic flagellates as potential grazers of heterotrophic bacteria and APP. In addition, the planktonic larvae of the pearl oyster Pinctada fucata graze on heterotrophic bacteria and
492 APP in Uchiumi Bay 共Tomaru et al., 2000兲. The abundance of ciliates in Uchiumi Bay, which are also graze on APP and bacteria, is usually low relative to those in other marine environments 共Ueno and Nakano, in preparation兲, suggesting ciliates are less important as grazers of the picoplankton in the bay. It needs to be identified which flagellates or larvae are grazers of picoplankton, and which microorganisms are the most important picoplankton grazers. We have demonstrated differences in response by APP and larger eukaryotic phytoplankton to intermittent nutrient supplies from bottom intrusion into a coastal sea, and reported that the larger eukaryotic phytoplankton in Uchiumi Bay were subjected to severe or moderate nitrogen limitation from May 2000 to May 2001, except during the bottom intrusion in summer 共June, July and August 2000兲 共Hashimoto and Nakano 2003兲. It is likely that the dominant organic matter cycling in the bay is due to the microbial food web through most of the year. Due to the occurrence of bottom intrusion, dominant organic matter cycling in the Uwa Sea may be changed by a shift in the energy-transport via microbial food web to a herbivorous food web. Painting et al. 共1993a兲 found high bacterial abundance during diatom bloom in the southern Benguela upwelling region, whereas the seasonal changing pattern of bacterial abundance was independent of those of larger eukaryotic phytoplankton in the present study 共Figure 4, Figure 5兲. The cause for this is still unclear, in the absence of information about changes in dominant food linkages in a given aquatic system, in relation to changes in its trophic state . The results of the present study can be applied to food web dynamics in varying environments such as upwelling areas in marine ecosystems.
Acknowledgements We thank K. Hyodo, T. Hirose and the staff of Uchiumi Institute of Oceanic and Fishery Science, and the students of Ehime University, N. Udaka, A. Murabe, M. Miyagaki, S, Kamata, T. Hashimoto, Y. Hotta, D. Ichinotsuka, H.Ueno and R. Asaumi for their help in field monitoring. Thanks are also due to Prof. Suzuki and other members of the Aquatic Biology and Ecology Laboratory of CMES, Ehime University, for their advice, discussions and encouragement throughout the study. We thank Dr. M. J. Morris for correction of our English and constructive comments on the manu-
script. The present study was partly supported by the Grant-in-Aid for Scientific Research No. 12308027, JSPS, and the Research Fund of coastal environment in Uchiumi Bay, Uchiumi Village, Ehime Prefecture.
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