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An Improved Model of Carbon and Nutrient Dynamics in the Microbial Food Web in Marine Enclosures

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An Improved Model of Carbon and Nutrient Dynamics in the Microbial Food Web in Marine Enclosures AQUATIC MICROBIAL ECOLOGY Vol. 14: 91-108.1998 Published January 2 Aquat Microb Ecol An improved model of carbon and nutrient dynamics in the microbial food web in marine enclosures 'Ecological Modelling Centre, Joint Department of Danish Hydraulic Institute and VKI, Agern Alle 5, DK-2970 Harsholrn, Denmark 'VKI, Agern All6 11, DK-2970 Harsholrn, Denmark 3National Environmental Research Institute, PO Box 358, Frederiksborgvej 399, DK-4000 Roskilde, Denmark ABSTRACT: A description of an improved dynamic simulation model of a marine enclosure 1s given. New features In the model are the inclusion of picoalgae and rnixotrophs; the ability of bacteria to take up dissolved inorganic nutrients directly; and, for the phytoplankton functional groups, the inclusion of luxury uptake and the decoupling of the nutrient uptake dynamics from carbon-assimilat~ondynamics. This last feature implies dynamically variable phosphorus/carbon and nitrogedcarbon ratios. The model was calibrated with experimental results from enclosure experiments carried out in Knebel Vig, a shallow microtidal land-locked fjord in Denmark, and verified with results from enclosure experi- ments in Hylsfjord, a deep and salinity-stratified Norwegian fjord. Both observations and model simu- lation~showed dominance of a microbial food web in control enclosures with low productivity. In N- and P-enriched enclosures a classical food web developed, while an intermediate system was found in N-, P- and Si-enriched enclosures. Mixotrophic flagellates were most important in the nutrient-limited control enclosures where they accounted for 49% of the pigmented biomass and about 48% of the primary production. Lumping the mixotrophs in the simulation model with either the autotrophic or the heterotrophic functional groups reduced total primary production by 74 %. Model-derived, time- averaged phosphorus budgets suggested that bacteria competed with algae for orthophosphate in the control enclosure, but not in the enclosure to which N and P had been added, where bacteria func- tioned as net mineralisers of phosphate. In the N, P and Si enclosure, bacteria took up only 10% of the amount of orthophosphate taken up by the primary producers, passing most of the organic phosphorus on to their grazers, the heterotrophic nanoflagellates, and mineralising only a small fraction directly. Inclusion of luxury nutrient uptake affected the simulation of the nutrient-enriched enclosures, while the decoupling of carbon and nutrient dynamics affected the simulation of the control enclosure. With- out these 2 processes it was not possible to simulate the carbon and nutrient dynamics in the different enclosures adequately with the same parameterisation. KEY WORDS: Microbial food web . Luxury uptake . Nutrient uptake . Nutrient cycles - Ecosystem model . Mesocosm INTRODUCTION model, making a dynamic simulation model that faith- fully reproduces the shifting pathways of carbon and The construction of an ecological model able to nutrients in the pelagic system while obeying the mass adapt its internal channelling of the C, N, P and Si conservation law is a complex affair, especially as the flows in the pelagic food web in response to perturba- bulk of the information on carbon and nutrient fluxes is tions in the availability and the partitioning of the indirect, in the form of biomass distributions and nutri- nutrients is one of the holy grails in ecological model- ent concentrations which by themselves are singularly ling. However, as easy as it is to construct a conceptual uninformative with regard to the underlying fluxes, of which the standing stocks and concentrations are the end product. 0 Inter-Research 1998 92 Aquat Slicrob E It is for these reasons that experimental setups and range of 4 different pathways in the marine planktonic mesocosm experiments are invaluable for the testing food web, from dominance by the herbivorous web, and improvement of ecological models (Baretta- coinciding with the classical food chain sensu Cushing Bekker et al. 1994, Escaravage et al. 1995, 1996, Black- (1989), through a multivorous web where microbial burn et al. 1996, Zweifel et al. 1996). Conclusions grazing is as significant as herbivorous grazing, to food based on the results of the simulations of marine enclo- webs increasingly dominated by grazing and recycling sures described by Baretta-Bekker et al. (1994) were within the microbial components. In effect Legendre & that (1) the biological resolution of the model, with Rassoulzadegan (1995) proposed the existence of a phytoplankton only comprising diatom and auto- generic pelagic food web with the different pathways trophic flagellate functional groups, was too coarse, as expanding or contracting in response to modulations in it included neither a mixotrophic functional group nor the nutrient and light-energy supply. picoalgae (Baretta-Bekker et al. 1994) and (2) the use In the present study the main objective was to of Michaelis-Menten nutrient kinetics in the model, improve the earlier model of mesocosm experiments which does not allow for intracellular nutrient storage described by Baretta-Bekker et al. (1994) into a model or luxury uptake of nutrients (Droop 1974, Nyholm that is capable of predicting the time evolution of the 1977), was a probable cause of discrepancies between biological constituents and the nutrient concentrations observed and model-predicted concentrations of nitro- as observed in short-term mesocosm experiments by gen and phosphorus. simulating the carbon and nutrient dynamics in nutri- Mixotrophic nanoflagellates are commonly found in ent-enriched as well as in nutrient-poor conditions. many different environments, and in some cases these The model described is based on a subset of the pigmented organisms contribute significantly to the ERSEM model, version 11. An overview of ERSEM is grazing of bacteria in lakes (Bird 91 Kalff 1986, Bennett given in Baretta et al. (1995). See Varela et al. (1995) et al. 1990) and in coastal marine environments (Hav- and Ebenhoh et al. (1997) for descriptions of the pri- skum & Riemann 1996). mary production module, Baretta-Bekker et al. (1995) In recent years, the topic of rnixotrophic nutrition in for the description of the microzooplankton module pelagic protists (flagellates and ciliates) has received and Broekhuizen et al. (1995) for the mesozooplankton increasing attention. In particular, the use of fluores- module. cently labelled particles as tracers for uptake has The model runs in the software environment improved the understanding of the role of phago- SESAME (Ruardij et al. 1995), on UNIX machines trophic phytoflagellates (Sanders 1991, Riemann et al. under Solaris. The conceptual time step is 1 d, thus all 1995). The combination of autotrophic and hetero- rate parameters have the unit d-l. SESAME uses adap- trophic nutrition in some protists provides an alterna- tive time-stepping, reducing the time step whenever tive route of material between microbial compartments any rate of change exceeds 0.5, thus minimising the in addition to the ones included in the more traditional numerical inaccuracy inherent in the used Eulerian concept of the microbial loop (e.g.Fenchel 1988). integration method. The minimum value the time step The fact that mixotrophs do not rely on just 1 mode of can attain is set at 1 X 10-6 d, which is about 0.09 S. nutrition gives them a competitive a.dvantage, espe- The model is calibrated with data from mesocosm cially under limiting conditions (e.g. low light or low experiments carried out in a small fjord in northeastern prey density), compared to strictly autotrophic or het- Denmark and verified with independent measure- erotrophic protists. The relative importance of the 2 ments from other mesocosm experiments carried out in nutrition modes, however, is largely unknown, since it the upper bracklsh layer of a fjord in southwestern tends to be species-specific and dependent on the Norway. environment (Sanders 1991).It has therefore been dif- ficult to generalise the importance of mixotrophs and ii~efactors controlling riatuia! populatio~s.As a conse- MATERIAL AND METHODS quence, there is a need for suitable models to predict the conditions under which mixotrophs may become Mesocosm experiments. The model is calibrated significant (Riemann et al. 1995, Thingstad et al. 1996) with data from mesocosm experiments carried out In and to examine their ecological role in microbial Knebel Vig, Denmark (56" 14' N, 10" 29' E), in the assemblages. period from 26 June to 8 July 1994. Basically, the The complex structure of the marine planktonic food experiments, performed m cylindl-ical enclosures with web allows for the dominance of strongly different a diameter of 1.75 m and a depth of 3 m, are the same components of the pelaglc community In interaction as those in 1991, described in Baretta-Bekker et al. with changes in the chemical and physical environ- (1994).The model was applied to 3 of the enclosures: ment. Legendre & Rassoulzadegan (1995) dscerned a 1 control and 2 of the nutrient-enriched ones, to which Baretta-Bekkei- et al.. An lmproved nlodel of carbon and nutrlent dynamics 93 -- - - --p N and P or N, P and Si had been added. Table 1 details Table 1. Dally addit~onof nutr~entsIn the form of inorganic the enrichment regimes. Initial values for the state nitrogen, phosphorus and silicate in mm01 m-3 to 2 enclosures variables were measured only In the control and were In the Knebel Vlg (Denmark)experiments, 1994 applied here to all 3 enclosures. The model was validated with measurements from Date N, P, Si enclosure N, P enclosure other mesocosm experiments carried out in the upper Np- P Si N P P p - - -- brackish layer of Hylsfjord (59" 30' N, Go 30' E), which 26 June 14 2 14 14 2 1s part of the Sandsfjord fjord system on the southwest- 27 June 14 2 14 14 2 ern coast of Norway, in the period from G to 13 July 28 June 14 2 14 14 2 1995. Data were used from 4 enclosures which, with a 29 June 14 2 14 14 2 30 June - - - diameter of 1 m and a depth of 2 m, were somewhat 1 July - - - smaller than those in Knebel Vig, enriched with 2 July 7 - - - nitrate, phosphate and glycine in different combina- 3 July 35 - - - - tions according to Table 2.
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