Home to diverse communities of plant and animal species, coastal zones are among the most biologically productive areas in the world. Coastal waters are linked to the upland basins that drain into them by the flow of water carrying sediments, organic matter and inorganic nutrients. Changes in human activity have an impact on these links; the removal of forests to make way for agriculture or residential development, for instance, tips the balance between organic matter and inorganic nutrients in the flux from the uplands into the coastal waters. Members of The Ecosystems Center's Land Margin Ecosystem Research (LMER) group are interested in understanding the effects of these changing inputs on the trophic structure of coastal food webs, especially the production of higher trophic levels, such as fish or shellfish.

Working with Meredith Hullar of Harvard University and Mark Benfield and Ee Lin Lim of the Woods Hole Oceanographic Institution, center staff members Linda Deegan, Anne Giblin, John Hobbie, Chuck Hopkinson, Joseph Vallino, Ishi Buffam, Robert Garritt and Jane Tucker carried out a field experiment during 1994 that was designed to test our understanding of how changing inputs of nutrients and organic matter influence the trophic structure of coastal waters. We were interested in determining how different levels of dissolved organic matter and dissolved inorganic nutrients altered food web dynamics and how much of the dissolved organic material supported higher trophic levels.

The experiment was set up in Woods Hole Great Harbor, where an old stone pier in front of the National Marine Fisheries Service facility provided a sheltered location. We submerged and filled four large transparent bags (roughly two meters across and three deep) with harbor water, creating mesocosms with typical populations of phytoplankton, bacteria, zooplankton and a larval fish called Atlantic silversides (Menidia menidia). The fish were added; the rest of the organisms were present in the harbor water. We excluded large fish and other predators from the mesocosms.

We designed several experimental treatments to examine the interaction of the microbial and planktonic food chains in the coastal food web. Inputs into coastal waters from natural terrestrial systems, such as forests, contain primarily organic matter. Organic matter must be consumed by bacteria before it can contribute to the production of higher trophic levels. Inorganic nutrients, on the other hand, bypass the microbial food chain and stimulate blooms of phytoplankton, which provide high-quality food for zooplankton, small invertebrates and shellfish. As forested lands in coastal watersheds are converted to farms and residential developments, the input of inorganic nutrients increases relative to the input of organic matter.

Each of the four mesocosms was treated differently. We added dissolved organic matter (DOM) to one bag, dissolved inorganic nutrients (DIN) to another and both DOM and DIN to a third. The fourth mesocosm served as a control. The added DOM was in the form of a strong, tea-colored solution, derived from soaking leaves in seawater for two weeks. Some dissolved nutrients were present in this solution. We added enough of this solution to bring the DOM concentration in the first and third bags up to a level that is typical of inputs from forested watersheds during spring runoff. For the DIN treatments, we added a solution containing nitrate, phosphate and silicate each day.

One of our major interests was in tracing the different sources of carbon from one trophic level to another. To do so, we used the ratio of carbon-13 (¹³C), a stable but rare isotope of carbon, to carbon-12 (¹²C), the common form of the element, as a means of tracing the passage of carbon from various sources through the food web. In order to describe this ratio, we use the delta (d) notation, in which the ratio of two isotopes in a sample is expressed as a per mil (‰) deviation from an agreed-upon standard value. Plankton in seawater and DOM from forested watersheds both have d ¹³C values around -25 ‰ to -30 ‰. Organisms at higher trophic levels have d ¹³C values that are roughly the same as their sources of food. In order increase our ability to differentiate carbon derived from phytoplankton from carbon derived from forest runoff, we added enough inorganic carbon enriched in ¹³C to all the experimental bags to elevate the d ¹³C value of the dissolved inorganic carbon in the water to +120 ‰. We anticipated that the phytoplankton in each of the mesocosms would take up the enriched inorganic carbon and exhibit d ¹³C values around +100 ‰.

If the zooplankton in the mesocosms consumed only the enriched phytoplankton, we would expect them to have d ¹³C values similar to their food. If they consumed only organisms that were dependent solely on the forest DOM, their d ¹³C value would remain around -30 ‰. Intermediate values would indicate that the zooplankton were consuming food derived from both sources.

The results of the experiment confirmed some of our hypotheses about the way estuarine food webs function. Phytoplankton biomass and production were highest in the two mesocosms with DIN and lowest in the control (Figure 1). During the first seven days, phytoplankton bloomed in all three experimental mesocosms. The nutrients, such as ammonium, that were added with the DOM were exhausted within the seven days, and phytoplankton biomass and production declined in the DOM mesocosm, although low levels of production were sustained throughout the experiment as the microbes released DIN during decomposition of DOM and the initial plankton bloom.

We observed that large phytoplankton cells were the primary producers under high nutrient conditions. In both of the mesocosms with added DIN, more than 50% of the primary production consisted of large-celled phytoplankton such as diatoms. In the control mesocosm and the one to which we added only DOM, on the other hand, small-celled algae made up most of the primary production.

We found that additions of both DOM and DIN, alone or together, stimulated the microbial food chain. Bacterial production was between seven and 20 times higher in the treated mesocosms than in the control, and biomass was between two eight times higher. Bacterial biomass and production were highest in the two mesocosms with DIN additions. Phytoplankton production and biomass were greatest in these two mesocosms, indicating that particulate and dissolved organic matter from the phytoplankton provide a high-quality source of food for the bacteria.

Zooplankton also responded to the increased food available in the mesocosms with the added nutrients as compared to the control or DOM-only mesocosms. Respiration measurements showed that zooplankton biomass was greatest in the two mesocosms that included DIN, intermediate in the DOM only mesocosm and very low in the control mesocosm. The large-celled phytoplankton provide high-quality food for the zooplankton directly, whereas the smaller-size phytoplankton enter a longer food chain that wastes far more energy.

Surprisingly little carbon from the DOM made it to the higher trophic levels. The larval fish tripled in weight in all the mesocosms over the course of the three-week experiment, which indicates that they were not limited by the availability of food (Figure 2a). As they grew, their d ¹³C values changed from -20 ‰ to around +50 ‰ (Figure 2b). During the same period, the d ¹³C values of the zooplankton in the DOM microcosm also shifted from -20 ‰ to + 50 ‰. Although we do not have all the results yet, these shifts toward the d ¹³C value of the phytoplankton in the experiment (+100 ‰) indicate that the efficient production of higher trophic levels in coastal ecosystems depends heavily on phytoplankton, which depend, in turn, on the supply of inorganic nutrients.

We confirmed our expectation that inorganic nutrients stimulate the type of production that provides more nourishment more readily to organisms at higher trophic levels and that organic matter alone is insufficient to stimulate "efficient" production. But this conclusion does not entitle us to say that high inputs of nutrients into coastal waters will increase fish production. If the level of nutrient inputs is too high, it can stimulate so much algal production that the zooplankton cannot consume enough to control the standing stock of phytoplankton. When the phytoplankton die, bacterial decomposition consumes oxygen.

Excess algal growth and low dissolved oxygen levels have an adverse effect on the growth and survival of fish. The coastal food web is delicately balanced. Continued production of higher trophic levels depends on sufficient nutrients to stimulate phytoplankton production but not so much that the ability of the system to transfer production up the food web is overwhelmed.