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Effects of Nutrients, Planktivorous Fish and Water Column Depth on Components of the Microbial Food Web

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Effects of Nutrients, Planktivorous Fish and Water Column Depth on Components of the Microbial Food Web AQUATIC MICROBIAL ECOLOGY Vol. 19: 67-80, 1999 Published September 6 Aquat Microb Ecol 1 l Effects of nutrients, planktivorous fish and water column depth on components of the microbial food web 'Ottawa-Carleton Institute of Biology, University of Ottawa, Ottawa, Ontario KIN 6N5, Canada 2~epartementde Sciences Biologiques, Universite de Montreal, Montreal. Quebec H3C 357, Canada 3National Water Research Insitute. Canada Center for Inland Waters, PO Box 5050, Burlington. Ontario L7R 4A6, Canada ABSTRACT: An experimental study was conducted uslng large enclosures to examine the effects of nutrients, presence of planktivorous fish, and depth of the water colun~non the components of the microbial food web. Enclosures (8 m in diameter) were installed, open to the sediments, at both 3.5 and 11 nl depths in Lac Croche, a small oligotrophic lake on the Canadian Shield The abundance of proto- zoans, including obligate heterotrophic flagellates (HNAN) and potentially mutotrophic flagellates (MIXO),was examined in relatlon to the abundance of thelr prey, both heterotrophlc bacteria (HBAC) and picocyanobactena (PPICO).HBAC levels increased over the summer and were s~gnificantlyhigher in the nutrient enriched enclosures. While HBAC dld not respond in a consistent manner to the pres- ence of fish, the effect of nutrients was greater when fish were present. HBAC levels did not differ slg- nificantly between the shallcw and deep enclosures. In contrast, PPICO were signlf~cantlydffected by all 3 independent variables, nutrients had a strong overall negative effect on abundance and the pres- ence of fish tended to Increase their abundance particularly in the shallow enclosures Similarly, nutri- ent additions resulted in sigruficantly lower HNAN levels, but neither the presence of fish nor depth of the water column slgniflcantly affected HNAN. However, the lowest average HNAN concentrations were in the deep nutrient enriched enclosures without fish, where the highest populatlons of Daphnia middendorffiana developed. MIXO were most abundant early In the season (exceeding HNAN) but declined significantly by mid-summer and were generally not as abundant as HNAN. MIXO levels were significantly lower in the nutrient enriched enclosures. Depth of the water column had a signifi- cant effect on MIXO, but MIXO levels were not affected m a consistent manner by the presence of fish. Experimental results did not demonstrate that Increases in nutnent levels would lead to Increases in HNAN as current empirical models imply. There was no increase in HNAN abundance related to Increased bacterial abundance. KEY WORDS: Microbial food web . Picoplankton. Nutrients . Zooplankton. Top-down control INTRODUCTION sive research (Fenchel 1987, Porter et al. 1988). Het- erotrophic nanoflagellates (HNAN) are generally the During the past decade, the ecological role of proto- most abundant protozoa in the euphotic zone of zoa in aquatic systems has become the focus of exten- aquatic systems and are now considered an important component of pelagic food webs (e.g. Azam et al. 1983, Present addresses: Sherr & Sherr 1984). Several studies have recognized 'New York City Dept. of Environmental Protection, Bureau these protozoa as the principal consumers of bacteria of Water Quality, Supply and Protection, Corona, New and picoplankton. They control bacterial populations York 11368-5107, USA through grazing and convert bacterial production into "'Ottawa-Carleton Institute of Biology, University of Ottawa, Ottawa, Ontario KIN 6N5, Canada larger particles, which can then be utilized as food by "Addressee for correspondence. larger protozoans and metazoans (e.g. Sherr & Sherr E-mail: [email protected] 1984, Andersen & Fenchel 1985, Sanders et al. 1989). O Inter-Research 1999 68 Aquat Microb Ecol 19: 67-80, 1999 Furthermore, HNAN play a key role in regulating piscivorous fish and large Daphnia species. However, nutrient flow through the microbial loop of aquatic sys- in experimental studies HNAN are not always affected tems. Substantial amounts of organic carbon, nitrogen, by Daphnia additions (Pace & Funke 1991). There is and phosphorus contained in their prey (picoplankton) also evidence for efficient predation on HNAN by are released into the environment as regenerated min- other metazoans such as rotifers and calanoid cope- erals (e.g. Goldman & Caron 1985). pods (e.g.Sanders et al. 1994, Jiirgens et al. 1996) and Several factors potentially regulate the abundance of by ciliates (Arndt 1993). HNAN. The abundance of prey may be the most A third factor is thermal stratification, which may important factor regulating HNAN seasonal levels have profound effects on the relative importance of the (Fenchel 1982). A close coupling between HNAN and classical versus microbial food web (Cushing 1989).In bacteria has been observed in several systems (e.g. stratified water small cells tend to dominate biomass Rassoulzadegan & Sheldon 1986) although not all (e.g. and primary production and hence energy flow Pick & Hamilton 1994, Simek et al. 1997). In turn, bac- through the microbial loop is theoretically more signif- terial abundance or productivity has been correlated icant (Porter et al. 1988, Kiarboe et al. 1990). In addi- with algal biomass or primary production over a wide tion, the relative importance of top-down versus bot- range of marine and freshwater systems (Bird & Kalff tom-up control may be quite different in shallow 1984, Cole et al. 1988). Berninger et al. (1991) de- versus deep lakes (Moss et al. 1994). scribed a significant correlation between bacterial In general, experimental tests of the role of nutrient abundance and HNAN abundance over a wide range supply versus predation in regulating HNAN have of freshwater systems, suggesting that system produc- been conducted in small containers or enclosures over tivity may be the most significant factor regulating short time periods (Riemann 1985, Pace & Funke 1991). HNAN. However, in temperate lakes of Eastern The effects of depth and thermal stratification on the Canada. HNAN abundance was not correlated with microbial loop in general have yet to be tested. In the bacterial abundance although total phosphorus ex- following study, large enclosures were used to investi- plained some of the variation observed between lakes gate the response of the microbial food web to altered (Tzaras & Pick 1994). A more extensive data analysis nutrients and overall food web structure. To address for a variety of aquatic systems by Gasol & Vaque the relative significance of nutrient loading (bottom- (1993) suggests that the relationship between HNAN up) or predatory (top-down) control on flagellate abun- and bacteria is not strong in any system. dance, we examined fertilized and unfertilized enclo- Secondly, the abundance of predators of HNAN may sures that either contained or excluded planktivorous be equally important. Zooplankton and ciliates are fish. These manipulations were examined in stratified both potential consumers of HNAN (Sanders & Porter (deep) versus continuously mixed (shallow) systems 1990). Seasonal declines in HNAN have been related within one lake. We examined the response of 4 main to increases in zooplankton (e.g.Jiirgens & Giide 1991, components of the microbial community: the hetero- Jiirgens 1994, Sanders et al. 1994) or ciliates (Weisse et trophic bacteria (HBAC), the photosynthetic pico- al. 1990). Experimental additions of Daphnia partially plankton (PPICO), which are also preyed on by proto- regulated HNAN abundance in lake container experi- zoan flagellates (e.g. Nagata 1988, Fahnenstiel et al. ments (Pace & Funke 1991). The correlation analyses 1991, Simek et al. 1997), the HNAN and potentially of Gasol & Vaque (1993) indicate that cladoceran mixotrophic flagellates (MIXO), which can also be abundance can explain a large fraction of the total important consumers of picoplankton (e.g. Porter 1988, variation in HNAN observed in lakes. Sanders & Porter 1988) as well as being frequently Because zooplankton community structure can be more abundant that HNAN in inland lakes (Pick & altered by fish planktivory (e.g. McQueen et al. 1986), Hamilton 1994). cascading effects on HNAN are possible. Rieman.n (1985) first showed experimentally that increases in planktivorous fish caused significant increases in MATERIALS AND METHODS HNAN. He attnbuted the increase to reduced preda- tion from 2 large cladoceran species (Daphnia cucul- Study site. The enclosures were installed in Lac lata and D. galeata). Subsequent enclosure experi- Croche (74" 00' N, 45'59' W), a small (4.82 ha), soft wa- men.ts confirmed these early results (Christoffersen et ter, slightly dystrophic lake located at the Station de Bi- al. 1993). In comparing 2 lakes wlth contrasting food ologie des Laurentides of the Universite de Montreal, ap- web structure, Vaque & Pace (1992) found that the lake proximately 70 km north of Montreal on the Canadian dominated by planktivorous fish (and containing small Shield. The lake has a pH of 6.3to 6.9 and dissolved or- cladoceran species) also contained the highest flagel- ganic carbon (DOC) levels range between 4 and 5 mg 1-' late abundance compared to the lake dominated by Spring total phosphorus levels average 10 pg I-'. Tzaras et al.: Nutrient, planktivorous fish and depth effects on mlcrobes The lake is dimictic, with a maximuin depth of 11.5 m 1988). Epilimnetic total phosphorus levels in the and a mean depth of 8.5 m. The thermocline is at ap- enriched enclosures were about 4 times higher than proximately
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