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Effects of the Zebra Mussel on Nitrogen Dynamics and the Microbial Community at the Sediment-Water Interface

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Effects of the Zebra Mussel on Nitrogen Dynamics and the Microbial Community at the Sediment-Water Interface AQUATIC MICROBIAL ECOLOGY Vol. 21: 187-194.2000 Published March 31 Aquat Microb Ecol 1 Effects of the zebra mussel on nitrogen dynamics and the microbial community at the sediment-water interface Peter J. Lavrentyevll*, Wayne S. ~ardner~l*, Longyuan Yang3 'University of Michigan. Cooperative Institute for Limnology and Ecosystem Research. 2200 Bonisteel Boulevard. Ann Arbor. Michigan 48109. USA 2National Oceanographic Atmospheric Administration, Great Lakes Environmental Research Laboratory, 2205 Commonwealth Boulevard, Ann Arbor, Michigan 48105, USA 'Chinese Academy of Sciences, Nanjing Institute of Geography and Limnology, 73 East Beijing Road, Nanjing, Jiangsu 21008, PR China ABSTRACT: A flow-through expenment was conducted on intact cores of sedunents from Saginaw Bay, Lake Huron, to examine how trophic interactions between filter-feeding bivalve mussels and microbial populations could affect nitrogen dynamics at the sediment-water interface. The zebra mus- sels used in this experiment removed a large proportion of protozoa and phytoplankton from the over- lying water, particularly heterotrophic nanoplankton (up to 82 %), while bacterial population~showed less change. A 3-fold decrease in the protozoan to bacterial carbon ratio corresponded to a 2.5-fold increase in relative ammonium removal rates as estimated from the dark loss of '5N-ammonium. Excre- tion by the bivalves also increased net ammonium flux to the water, thus elevating the total calculated area1 ammonium removal rates to about 6-fold over rates observed in the control treatment. These data suggest that filter-feedng bivalves may significantly affect nitrogen transformation rates near the sed- iment-water interface by excreting ammonium and altering the microbial food web structure at the sediment-water interface. KEY WORDS: Nitrogen . Microbial food web . Sediment-water interface . Bivalve mussels INTRODUCTION If oxygen is present, as often is the case in shallow waters, a portion of ammonium may be oxidized to The sediment-water interface is a region of active nitrate (Ward 1986). In turn, the nitrate may be com- biological and biogeochernical processes, such as labile pletely or partially denitrified to nitrogen gas in adja- organic matter biodegradation and ammonium pro- cent sites (Seitzinger 1988). Understanding the mecha- duction in shallow coastal systems. Under such condi- nisms that control the extent of N transformations at tions, kinetic diffusion-reaction models based on equi- the sediment-water interface is important, because libration of ammonium between the sediments and these processes can affect the amount of mineralized N pore water do not adequately predict actual ammo- that is ultimately available to primary producers or lost nium flux into overlying waters (Ullman & Aller 1989). through denitrification. Trophic cascades involving bacterivorous protozoa can affect community N regeneration rates (Suzuki et Present addresses: al. 1996) and bacterial community structure in the water 'University of Akron, Department of Biology, Akron, Ohio 44325-3908, USA. E-mail: [email protected] column (Jiirgens & Giide 1994). Furthermore, plank- "University of Texas at Austin, Marine Science Institute, 750 tonic bacterivorous protozoa can inhibit the biogeo- Channel View Drive, Port Aransas, Texas 78373, USA chemical process of nitrification, directly by reducing 0 Inter-Research 2000 188 Aquat Microb Ecol21: 187-194,2000 bacterial numbers and indirectly by forcing bacteria to MATERIAL AND METHODS grow in colonies, whereas predation by larger zoo- plankton diminishes these effects (Lavrentyev et al. Material for this study was collected from Saginaw 1997). The important role of the bottom-dwelling pro- Bay, a large (about 82 km long and 42 km wide) bay tozoa in consuming heterotrophic bacterial production extending off the western edge of Lake Huron. The (e.g. Bak et al. 1995) supports the idea that similar cas- shallow (1 to 3.5 m depth) inner bay receives large cading trophic effects on nitrogen transformation may inflows of enriched waters from the Saginaw River. take place at the sediment-water interface. Here, rnicro- Since 1991, the zebra mussel has heavily infested the organisms are involved in complex interactions with inner bay (Nalepa et al. 1995). other benthic organisms that have significant effects Intact cores of sediments and the overlying water on nitrogen transformations (Dame et al. 1984, 1991, were collected by SCUBA divers from a site near Au Henriksen & Kemp 1988). Gres Point (43'56'N, 83 "52'W) on June 30, 1995. One of these organisms is the zebra mussel Dreis- These samples were taken using 76 mm internal diam- sena polymorpha, an invasive filter-feeding bivalve that eter plastic tubes. Simultaneously, several pebbles col- alters the structure of food webs in shallow areas by onized by the zebra mussel were collected for experi- fiitering particies (e.g. Naiepa et al. 1995) and excret- mentai additions. Severai 20 i carboys or surface water ing nutrients (Gardner et al. 1995b. Binelli et al. 1997). from the same site were collected to supply a flow- In this study, we examined how trophic interactions, through system. The samples were transported to the induced by zebra mussels, can modify the microbial laboratory in insulated coolers within a few hours after food web structure and nitrogen transformations at the collection. sediment-water interface. The sedirnents were placed in a system consisting Studying trophic interactions and nutrient transfor- of the cores (in the original collection tubes), a clear mations involving microorganisms at the sediment- polycarbonate vessel with intake lake water, a Techni- water interface presents methodological difficulties. con peristaltic pump, and an outflow collection vessel The use of a I5N tracer is necessary to study N dynam- (Fig. 1). This laminar flow system is an improved and ics because of close coupling between ammonium re- larger version of the flow-cell described earlier (Gard- generation, nitrification, and denitrification. The mass ner et al. 1991).It was designed with an 0-ring seal and analysis techniques for 15N require large sample vol- plunger that could be lowered to the desired position umes and involve multi-step sample preparations that without disturbing the surface sedirnents. The overflow increase the risk of contamination. The physical, che- tube released water as the plunger was positioned but mical and biological nature of the sedimentary matrix was closed during operation. Water was pumped over is impossible to replicate in the laboratory; yet, the the sediment surface at a rate of 1 m1 rnin-l. maintenance of this structure is crucial to many ben- The pebbles holding the zebra mussels were of dif- thic processes (Miller-Way & Twilley 1996).The neces- ferent size and shape and had large amounts of peri- sity to maintain sediment integrity during an experi- phyton on them. Mussels were removed from the peb- mental incubation huts the application of conventional bles by cutting the byssal threads with a razor blade size-fractionation and dilution techniques that are com- monly used to modify food web structure in planktonic Hand'e Overflow tube Inflow - 0 studies. Further, the presence of meroplanktonic pro- tozoa, which are able to migrate freely between sedi- ments and the water column, may greatly diminish the Outflow effects of experimental manipulations with inlet water in such studies. +- 0-ring The purpose of this study was to examine how trophic + Lake interactions between filter-feeding bivalve mussels and water I microbial populations could change nitrogen dynamics in controlled experimental systems using intact sedi- ments. To simulate a trophic cascade, we used the ri zebra mussel as a 'biological particle filter' in a sedi- ment core continuous flow cell. We used this approach in combination with high performance liquid chromato- U graphic analysis of ammonium concentration and atom Intake water Collection vessel % 15N to test the hypothesis that cascading trophic Fig. 1. The continuous flow through system. The diameter of effects involving bacterivorous protists affect nitrogen the core was 76 mm. The flow rate for the unfiltered water transformation at the sediment-water interface. was 1 m1 mix' Lavrentyev et al.: Casce~dlng effects on N dynamics 189 and rinsed with bay water to remove periphyton before passage across the dark core should not have ex- they were used in the experiment. Two adult mussels, ceeded that occurring in the inlet water held under shell length 22.3 mm * 0.69 SE, were added to each light/dark conditions. Therefore, the observed differ- triplicate core. By the time the system had reached ences in 15NH4+concentrations between the inflow and steady state, the zebra mussels remained either on the outflow waters were assumed to result from microbial top of the sedlments or attached to the side of the processes at or near the sediment-water interface. core tube above the sediment surface. Thus, they were Results from the flow-through core system, without positioned to filter overlying water rather than pore (incubation Days 2, 3, and 4) and with (incubation water. All zebra mussels remained alive during the Days 5, 6, and 7) I5NH4+additions, were used to cal- experiment and were still filtering water at the end of culate ammonium removal rates. Successive results the incubation. from each core were averaged before (n = 3) and after The cores and the inflow water from the sample site (n = 3) addition of I5NH4+to yield core-specific
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