ICES 2008 Theme Session A. ICES CM 2008/A:01 The role of the microbial food web in ecosystem-based management. Michael R. Heath, Marine Laboratory, Aberdeen, UK John H. Steele, Woods Hole Oceanogr. Instn., USA Abstract The present focus on ecosystem-based management (EBM) for fisheries has produced much work on budgets for nutrient or energy flow through ecosystems; usually with emphasis on the higher trophic levels. Some end-to-end studies use the ratios of fish yield to net primary production as a system index, but this ratio is very variable and can reflect differences in the factors determining nutrient recycling within the lower trophic levels, rather than stresses on the upper trophic components. We argue that explicit consideration of these physical, biogeochemical and ecological processes is essential if we are to understand the constraints on overall system productivity and the causes of changes in this productivity. We illustrate these issues with comparative analyses of the Georges Bank and the North Sea ecosystems. Contact author: John Steele: Woods Hole Oceanographic Institution, Woods Hole MA 02543, USA. [Tel. 508 289 2220: Fax 508 457 2184: Email: [email protected].] Introduction The interest in ecosystem-based management (EBM) has created a need for a variety of end-to-end representations of marine food webs in order to explain the community production and diversity of harvestable trophic levels, rather than just the dynamics of individual species in isolation. One approach has been to empirically relate higher trophic level production to primary production, so that spatial and temporal patterns in primary production can then be used as a basis for assessing the maximum potential fishery yield. There is considerable spatially and temporally resolved information on rates of net or total annual primary production by phytoplankton (TPP) based on a combination of remotely sensed color data and experimental measures using tracer (14C) uptake during incubations. However, relationships between primary and fish production seem to vary by an order of magnitude, Table 1. This variability may be partly due to differences in the way fish production is calculated, but must also indicate large variability in the efficiency with which primary production is transmitted up the food web. Its is clear that use of this approach as a basis for EBM requires a better understanding of the food web structure and function. There are a large number of factors which may influence the efficiency of transfer of TPP up the food web. Intuitively, we might expect that the most influential are likely to be 1 those at the lower trophic levels. Systematic variability in the complexity of the lower trophic level food web has the capacity to alter the effective trophic status of higher trophic levels and affect metabolic losses during the transfer of energy from primary producers to fish. Recognition of this is embodied in the concepts of “new” and “recycled” production (NP and RP), developed from the results of biogeochemical studies of mid-high latitude nitrogen limited open ocean ecosystems, particularly during the JGOFS programme. New production in the ocean The water column in the open ocean may be several km deep, but there is sufficient light for photosynthesis in only a thin layer (50-100m) at the surface (down to 0.1-1% of the sea surface irradiance). We refer to this as the photic zone. All of the dissolved inorganic nitrogen which is present as nitrate in the photic zone at the end of the winter is converted into living, and then dead particulate form as a result of photosynthesis, grazing and predation in the spring and summer. Dead particulate matter sinks out of the photic zone and disappears into the deep ocean. The depletion of nitrate in the photic zone sets up a vertical concentration gradient and nitrate diffuses from the underlying waters into the photic zone, supporting additional particulate matter production and export to the deep ocean, until declining irradiance in the autumn curtails photosynthesis. During the winter, vertical mixing recharges the photic zone with nitrate from the underlying waters. If the annual cycle of nitrogen in the photic zone is stationary, then the annual integrated vertical mixing and diffusion flux of nitrate into the photic zone from deep water must equal the annual particulate production of the photic zone food web and the sinking flux of detritus to the deep ocean. We refer to the primary production equivalent to the annual vertical mixing and diffusion flux as NP. However, NP does not equal TPP, because in the process of metabolizing the algal biomass equivalent to NP, the grazer and predator community in the photic zone excretes ammonia, which is then available to support additional primary production. We refer to the component of TPP supported by ammonia excreted by the heterotroph community as RP, and TPP = NP + RP. Remineralisation and nitrification of the particulate matter sinking out of the photic zone occurs deep in the ocean and contributes to the pool of deep ocean nitrate. But, since this pool is large compared to the annual export flux from the photic zone, the effective recycling rate of nutrient back to the surface waters is extremely slow (on the order of hundreds of years) and the space scales correspondingly large. Thus there is a clear disconnection between the very long term cycling of nutrient between the deep ocean and the photic zone, and short term dynamics of nutrient uptake by autotrophs and excretion of ammonia by heterotrophs. The ability to directly measure uptake rates of nitrate and ammonia using the stable isotope 15N incubation techniques provided a means of evaluating the relative importance of new and recycled production, and gave rise to the term “f-ratio”, defined as new/total production and estimated experimentally from f = NP/TPP = NO3 uptake/((NO3 + NH4) uptake) 2 For much of the open ocean 0.1 < f < 0.5 One reason for the wide-spread use of the f-ratio in relation to open ocean biogeochemistry was the general conclusion from observations that the f-ratio increase monotonically with the rate of TPP – the greater TPP the greater the fraction that is new production. This provided the basis for “global” relations between the f-ratio, temperature and TPP (Laws et al, 2000) which have been used to create global inventories of carbon flux to the deep ocean. In this paper we focus on the idea that the concept of NP could provide a closer relationship with integrated food web production and fisheries yield, than TPP. However, should we expect the generalizations and relationships established from ocean studies to hold for shelf regions? Are the concepts of NP and the f-ratio useful in such environments? Measures of Production in shelf seas The main fisheries interest in rates of primary production is in shelf seas rather than the open ocean. Hence, the concept of new versus total production has also been applied to shelf ecosystems (Richardson et al, 1998; Bisagni, 2003; Heath and Beare, 2008). However, there are a number of key differences. In shallow coastal waters the photic zone may extend to the seabed and hence there is no separation in either space or time of the processes of nitrate uptake, and the mineralization and nitrification of organic nitrogen back to nitrate, such as exists in the ocean. Nitrate production, together with inputs from rivers, atmospheric deposition, anthropogenic discharges and horizontal mixing occur throughout the year in the photic zone. In addition, the process of denitrification which involves the microbial utilization of nitrate as a source of oxygen in anaerobic environments and the release of gaseous nitrogen to the atmosphere, is a potentally significant loss term in shallow waters. In estuarine systems in particular, denitrification is a very significant term in the nitrogen budget. In the ocean, denitrification must be confined to deep waters where it cannot compete with phytoplankton for the available nitrate. The dynamics of nitrate concentration in the coastal water column will therefore be complicated, and reflect the balance between external inputs, competition between phytoplankton and nitrifying bacteria for the ammonia produced by remineralisation of dead organic matter, and between phytoplankton and denitrifying bacteria for nitrate. We could consider the annual influx of external dissolved inorganic nitrogen plus the annual mineralisation flux from dead matter to ammonia as being equivalent to NP in the ocean. But, what then is the shallow shelf equivalent of RP? Ammonia excreted by herbivores and predators in the food web (the metabolic consequence of herbivorous grazing and predation) is indistinguishable from the mineralization products of dead organic material. Hence, some 3 of the autotrophic nitrate uptake in shallow coastal waters may be equivalent to RP in the ocean model, and some of the ammonia uptake may be equivalent to NP. As one moves out from shallow coastal waters into deeper shelf areas, the space-time separation between the nitrogen uptake and recycling systems should begin to emerge, as the photic zone thickness becomes a smaller fraction of the total water column depth, and the near-seabed layers become more isolated from the surface. Nevertheless, its is clear that the simple definitions of new production and the f-ratio developed from open ocean studies, although potentially useful on the shelf, do not obviously provide a simple explanation of yields by shelf sea higher trophic levels. It is necessary to consider the structure of the microbial food web as a function of the physical topography of the sea bed in any particular region. We use the schematic in Fig. 2 to illustrate the complexity of nitrogen dynamics on high latitude shelves such as Georges Bank or the North Sea.