sign in sign up
<<
Home , Biomass (ecology), Dominance (ecology), Habitat, Lake ecosystem, Microbial food web, Microbial loop

New Approaches

Microbial Webs & Management

Karl Havens and John

cientists and managers ’s position in the . X magnification under a ) dealing with the open occurring at lower trophic are prokaryotic cells that represent one (pelagic) region of and levels (e.g., and ) of the first and simplest forms of often focus on two are near the “bottom” of the food web, on the . Most are heterotrophic, componentsS when considering water where and first enter meaning that they require organic quality or – the suspended the . Organisms occurring at sources of , however, some can () and the suspended higher trophic levels (e.g., synthesize carbon by or (zooplankton). This is for good and ) are closer to the top of the food . The blue- reason. Phytoplankton is the component web, i.e., near the biological destination of () actually are bacteria, but responsible for noxious algal blooms and the energy and nutrients. We also use the for the purpose of this discussion, are it often is the target of reduction more familiar term trophic state, however not considered part of the MFW because strategies or other in-lake management only in the context of degree of nutrient they more like phytoplankton solutions such as the application of enrichment. in the . Flagellates algaecide. Zooplankton is the component (Figure 1c), larger in size (typically 5 that provides the food for Who Discovered the to 10 µm) than bacteria but still very most larval fish and for adults of many ? small compared to zooplankton, are pelagic . Lake management that Although the concept of the MFW that similarly include species explicitly considers the pelagic food web may be new to lake managers, its that are – however, some uses approaches generally referred to potentially important role in the are “myxotrophs,” meaning that they can as – where the goal is was recognized as early as the 1940s, carry out photosynthesis and make use of to reduce the of phytoplankton when Lindeman (1942) hypothesized organic sources of carbon. by creating a situation that favors the that bacteria transfer energy to higher Flagellates are named for their of large efficient zooplankton trophic levels in the of of locomotion – the – such as that can graze the lakes and . A Polish ecologist, which may occur individually, as a pair, noxious algae. Z.M. Gliwicz, further elaborated on or in some atypical cases as three units. That these food web manipulations pathways of carbon and , The flagellum is a complex structure often are not successful (DeMelo et al. postulating that the link between bacteria largely comprised of tubes of that 1992), is due in part to additional food and zooplankton becomes predominant, is able to synchronously beat in order to web complexity beyond just algae, vs. algae to zooplankton, in lakes as move the through the water. zooplankton and fish. In particular, a large they become more heavily enriched with (Figure 1d-f), the largest members of portion of the biomass, nutrient cycling, nutrients (Gliwicz 1969). The full scope the MFW (typically 20 to 50 µm), also and energy transfer in the pelagic food of the MFW, as we know it today, was are eukaryotic, and for the most part are web involves plankton components in a described by a marine scientist (Pomeroy heterotrophs. Their name comes from different pathway than the aforementioned 1974). In the late 1980s, the MFW was the fact that the cell surface is covered grazing food chain, including bacteria and widely studied in lakes and linkages made with fine cilia (each structurally similar a variety of different . with , food web to a flagellum) that beat in synchrony to The aim of this paper is to describe efficiency, and water quality. propel the through the water and/ this microbial food web (MFW), identify or to generate feeding currents to capture its major components and their role in Who are the Major Players in the smaller food particles. the , and discuss how Microbial Food Web? knowledge about the MFW can be helpful The MFW is comprised of three How Do They Interact as a Web? in guiding lake management. major components – bacteria, flagellates, The components of the MFW are and ciliates. Bacteria (Figure 1a-b), interconnected as part of a complex Trophic Levels and Trophic States ranging in size from about 0.5 to 2 µm (a network (Figure 2), in which organic In this paper the term µm is one millionth of a meter and cells carbon and energy are captured and is used in a context that considers an of this size are visible only at about 1,000 transferred to higher trophic levels

32 Summer 2010 / LAKELINE very fine particles (e.g., and a b certain cladocerans including Daphnia), or they can be grazed by flagellates and/ or ciliates in the MFW. Flagellates in turn are a food source for ciliates, rotifers, and many of the larger zooplankton. Ciliates are consumed by larger zooplankton, such as calanoid , that can graze large food particles. Ultimately, the MFW transfers carbon and energy from the base of the food web (bacteria) to the top (zooplankton and fish). Early in the investigation of the marine MFW a controversy developed as to whether it functioned as a “link or sink” for carbon – the rationale for c d the sink argument being that much of the recaptured carbon is lost through in the many steps in the longer chains (Ducklow et al. 1986). However, it was soon identified that the grazing food chain has a similarly low efficiency (Sherr et al. 1987). Thus, a reasonable way to look at the MFW is that like the grazing food chain, it is inefficient, however, it serves an important function of recapturing what otherwise would be lost carbon and energy. A considerable amount of the nutrient recycling that occurs in the pelagic zone also happens within the MFW, as and e f excreted by algae and zooplankton are picked up by bacteria and transferred upward in this web.

Does the Importance of the MFW Change with Lake Trophic State? In general, the importance of the MFW, whether measured as the percent of plankton biomass associated with bacteria, flagellates, and ciliates, or the percent of carbon and energy flow, has a unimodal relationship with lake trophic state – with greatest importance in ultra-oligotrophic lakes and hypereutrophic lakes, and Figure 1. Photomicrographs of representative components of the microbial food web of a lake or lowest importance in mesotrophic : (a-b) rod-shaped bacteria from photographed at 2000X, (c) from lakes (Stockner et al. 1989; Weisse and Lake Erie photographed at 2000X, (d) the Cyclidium sp. from Lake Erie photographed at Stockner 1992). There are, however, 2000X, (e) the ciliate Strombidium sp. from Lake Powell photographed at 630X, (f) the ciliate exceptions. Lakes in the mesotrophic Codonella cratera from Lake Okeechobee photographed at 400X. Scale bar is 10 µm. Photographed by Kyle Scotese, Teodoro Rosati, Jeff Johansen, and John Beaver. range that receive water with a high organic (humic) content will tend to support high rates of bacterial (zooplankton and fish) in the lake released into the lake water. Bacteria and may have a food web that is ecosystem. When phytoplankton carry can incorporate some of this carbon into predominantly microbial (Tranvik 1992). out photosynthesis, they fix dissolved their own biomass, thereby recapturing Ultra-oligotrophic lakes, which largely

CO2 from the water into organic carbon carbon into the food web that otherwise have been investigated in Boreal regions, (glucose and subsequently other would have been lost. Subsequently, typically have much of their primary ), and during their the bacteria may be directly grazed by productivity associated with bacteria-sized and death, much of this fixed carbon is zooplankton that has the ability to filter phytoplankton called pico-plankton and

Summer 2010 / LAKELINE 33 How is this Information Important for Lake Management? The importance of plankton food web structure to fisheries productivity was identified in the late 1980s and subsequently that information was widely applied in fisheries management. This work predominantly occurred in Canada, where John Stockner and his colleagues (Stockner and Shortreed 1989) documented that ultra-oligotrophic lakes in British Columbia, with MFW Macro-Zooplankton dominance and associated long food chains, had low efficiency in energy transfer (as noted above, because of many steps in the chains), and supported low fish productivity compared with oligotrophic lakes were the grazing food chain was predominant and fish Micro-Zooplankton productivity was higher. This information was part of the scientific foundation (the other part being a net loss of nutrients due to over-fishing that reduced return of fish to spawning grounds) for large-scale Protozoa fertilization of ultra-oligotrophic lakes, aimed at increasing algal productivity and enhancing the relative biomass of larger algae that could be directly grazed by zooplankton. From the standpoint of Bacteria Phytoplankton increased fisheries productivity and the associated socio-economic benefits this Figure 2. Food web diagram showing trophic links between the various components of the program was a great success (Stockner traditional grazing food chain (green arrows) and the microbial food web (brown arrows), and and MacIsaac 1998). subsequent links to fish. Carbon can enter this food web in two ways – by photosynthesis carried Lake managers more often are out by phytoplankton and certain flagellates, and by uptake of by concerned with an excess of nutrients bacteria. rather than a lack thereof, and are engaged in projects to reduce nutrient inputs their dominant zooplankton there is a tendency for fish densities in order to reduce algal blooms, and/ is copepods that cannot graze such small and the associated pressure or conduct in-lake measures to enhance food particles. In those lakes the MFW on zooplankton to increase as species water quality and fisheries quality. plays a critical role where flagellates and like and gizzard shad become Because of the inefficient plankton food ciliates “package” the energy of the pico- increasingly dominant. This reduces the web and loss of summer refuges from plankton into particles large enough to be biomass of large effective zooplankton warm surface , hyper-eutrophic available to the copepods. In mesotrophic grazers such as Daphnia, leaving a lakes often lose their piscivorous fish lakes, a typical situation is dominance dominated by smaller taxa (e.g., pike), which in turn releases smaller of the phytoplankton by moderate sized including rotifers, small cladocerans omnivorous fish from predation leading to , greens and cryptophytes, (e.g., Bosmina, Chydorus), and copepods greater grazing pressure on zooplankton and cladocerans such as Daphnia that that have escape maneuvers. At the same (Persson et al. 1988). The coincidence of can directly graze them. Under these time, the phytoplankton community shifts high fish predation and -green circumstances, the MFW is present but toward increasing dominance by large algae results in small grazers that cannot plays a lesser role in carbon and energy filamentous and colonial blue-greens that eat the algae and therefore must rely on transfer than the grazing food chain. As are too large for the small zooplankton to the inefficient MFW. One strategy that lakes undergo and proceed directly consume. This situation sets up may be helpful to make such more along the gradient from mesotrophic to the MFW as the main route for carbon efficient, under certain circumstances and eutrophic to hypereutrophic, two things and energy flow, as bacteria sequester in combination with nutrient reduction, is occur, leading to a plankton food web in carbon excreted by the algae and transfer biomanipulation – for example, stocking which the MFW is predominant. First, it upward to the zooplankton via flagellate lakes with and/or removing and ciliate grazers.

34 Summer 2010 / LAKELINE plantivores and to reduce and transfer some of it upwards to fish Sherr, E.B., B.F. Sherr and L.J. Albright. grazing pressure on zooplankton and via protozoa and small zooplankton. An 1987. Bacteria: Link or sink? Science allow large species such as Daphnia to understanding of this food web and how 235:88. become abundant (Figure 3). it can be manipulated has been used to Stockner, J.G. and K.S. Shortreed. When biomanipulation is successful successfully address low productivity 1989. Algal production (and admittedly it does not always work), of fisheries in ultra-oligotrophic lakes and contribution to food webs in a part of that success is associated with and can potentially help lake managers oligotrophic British Columbia lakes. an increase in the relative importance achieve a successful enhancement of Hydrobiologia, 175:151-166. of the grazing food chain vs. the MFW. fisheries and water quality in eutrophic Stockner, J.G. and E.A. MacIsaac. 1998. This reflects the fact thatDaphnia can lakes where biomanipulation methods are British Columbia Lake Enrichment graze a wide range of plankton particles, under consideration. Programme: Two decades of from the smallest bacteria up to relatively enrichment for Sockeye . large ciliates and phytoplankton. This References Regulated : Research and “short-circuits” the MFW and results in a Crisman, T.L. and J.R. Beaver. Management, 12:547-561. much more efficient food web in regard 1990. Applicability of planktonic Tranvik, L.J. 1992. Allochthonous to supporting continued productivity of biomanipulation for managing dissolved as an energy fish. The trick, of course, is maintaining eutrophication in the subtropics. source for pelagic bacteria and the enhanced piscivores/ ratio, Hydrobiologia, 200:177-181. the concept of the . which might be an ongoing process in DeMelo, R., R. France and D.J. McQueen. Hydrobiologia, 229:107-114. temperate lakes if continued high nutrient 1992. Biomanipulation: Hit or myth? Weisse, T. and J.G. Stockner. 1992. inputs and algal blooms lead to anoxic or and , 37:192- Eutrophication: The role of microbial hypolimnetic waters and lack of 207. food webs. Memoirs Institut Italiano a summer from high epilimnetic Ducklow, H.W., D.A. Purdie, P.J.L. Idrobiologia, 52:133-150. water . It is not an effective Williams and J.M. Davies. 1986. process in the subtropics where large : A sink for carbon in Daphnia do not occur, cyanobacteria are a coastal marine plankton community. Karl Havens is director abundant, and the MFW is quite important Science, 232:865-867. of the Florida Grant (Crisman and Beaver 1990). Lindeman, R.L. 1942. The trophic- College Program at the dynamic aspect of . Ecology, University of Florida, Summary 23:399-418. Gainesville, FL (e-mail: In addition to the traditionally Persson, L., G. Andersson, S.F. Hamrin [email protected]). He recognized algal-zooplankton “grazing and L. Johansson. 1988. Predator has conducted research food chain,” the plankton of lakes and regulation and dealing with plankton reservoirs includes a more complex along the productivity gradient of food webs since the early microbial food web where bacteria take up temperate lake . Pp. 45- 1980s, and has published over 140 journal dissolved organic carbon from the water 65. In: S.R. Carpenter (Ed.), Complex articles, book chapters and review papers. (carbon released from algae excretion or Interactions in Lake Communities, He received his Ph.D. and MS degrees from carbon entering from outside the lake) Springer-Verlag, NY. West Virginia University and his BA degree from the State University of NY at Buffalo.

a Bosmina b Daphnia John Beaver is President of BSA Environmental Services in Beachwood, Ohio bacteria flagellates bacteria (e-mail: j.beaver@bsaenv. com). He is an aquatic ecologist specializing in North American lake water quality. Dr. CO DOC CO DOC 2 2 Beaver has authored approximately 40 referred journal articles related to aquatic and limnology in the scientific Figure 3. Two simple food web diagrams, showing cases of (a) low efficiency of carbon and literature. He received a Ph.D. and MS from energy transfer when small(a) zooplankton co-occur with large inedible algae; (b)and (b) high the University of Florida in Environmental efficiency of carbon and energy transfer when large Daphnia co-occur with edible algae. From a Engineering Sciences and a BS from fisheries or water quality standpoint, condition (b) is usually desired. CO2 represents the inorganic carbon taken up by algal photosynthesis and DOC is dissolved organic carbon excreted by algae. Jacksonville University in . x This is a highly simplified diagram and neither respiratory carbon losses nor release of DOC from zooplankton during feeding and excretion are shown.

Summer 2010 / LAKELINE 35