Complex interactions between autotrophs in shallow marine and freshwater ecosystems: implications for community responses to nutrient stress
Introduction
Aquatic ecosystems around the world have been heavily impacted by discharges of nutrients from human activities, including point sources of urban, residential, and industrial pollution, and non-point sources of agricultural pollution. Carpenter et al. (2000, p. 752) noted that cultural eutrophication (enrichment with nutrients from human sources) is “a widespread and growing problem of lakes, rivers, estuaries, and coastal oceans.” Problems associated with excess nutrient inputs have been documented for freshwater lakes, rivers, wetlands, and the coastal marine environment (Smith et al., 1999).
Phosphorus (P) and nitrogen (N) are the nutrients most often limiting to autotrophs in freshwater and marine ecosystems (Schindler, 1977, Heckey and Kilham, 1988, Vitousek and Howarth, 1991, Downing , 1997). When lakes, rivers, or estuaries receive additional inputs of these nutrients from anthropogenic sources, there are generally increases in the biomass of autotrophs, and sometimes dramatic changes in taxonomic structure and functional groups (Valiela et al., 1997a, Smith et al., 1999, Philippart et al., 2000). These changes can radiate upwards through the food web, affecting primary and secondary consumers (e.g. Valiela et al., 1997a, Moeller et al., 1998). Excessive nutrient loading can also lead to phenomena such as harmful algal blooms (Paerl, 1988, Burkholder and Glasgow, 1997).
Many aquatic ecosystems that are impacted by nutrients are shallow, and in contrast to deep plankton-dominated ecosystems they are capable of supporting a variety of autotrophs. These include: vascular plants; algae attached to plants, sediments, rocks, and other substrata; macroalgae; and phytoplankton. These autotrophs compete for nutrients, light, and space, and have other complex ecological interactions that may influence how the ecosystem as a whole responds to nutrient stress.
Conceptual models have been developed to describe changes in the relative biomass of plants, benthic algae, and phytoplankton as a function of nutrient loading and underwater irradiance. The model of Sand-Jensen and Borum (1991) predicts that in shallow lakes and estuaries with low nutrient availability in the water, benthic algae and vascular plants will dominate due to their ability to sequester nutrients from the sediments. In nutrient-enriched waters, however, phytoplankton will dominate because they rapidly sequester water column nutrients, increase in biomass, and shade the benthic algae and plants. Valiela et al. (1997a) expanded this model to explicitly consider benthic macroalgal mats. They predicted that with increased nutrient loading, macroalgae will be favored over vascular plants because they have: (1) a lower compensation irradiance for growth; (2) more rapid uptake of N, which typically is the primary limiting nutrient in estuaries (Howarth, 1988); and (3) more rapid growth. Macroalgae are predicted to form canopies that shade, and eventually kill, vascular plants. At the highest rates of nutrient loading, phytoplankton are predicted to dominate because they have an even lower compensation irradiance, nutrient uptake, and growth rates than benthic algae.
This paper presents four case studies that independently test these models or provide information about how other complex interactions between autotrophs can affect ecosystem responses to cultural eutrophication.
Section snippets
Case study 1 — effect of macroalgal shading on eelgrass (Zostera marina) production in a coastal estuary (Waquoit Bay, USA)
In the region of Cape Cod, MA, septic systems have become a major source of N loading to coastal ecosystems. As noted by Valiela et al. (1997b) and others, increased inputs of N can cause a suite of changes in estuaries, including macroalgal blooms. Observational evidence indicates that the thick canopies of macroalgae that accumulate on the bottom of receiving estuaries can shade and eventually replace seagrass beds (Duarte, 1995). A loss of eelgrass (Z. marina) has coincided, for example,
Case study 2 — the influence of macroalgae on dissolved organic N fluxes in a shallow coastal lagoon (Hog Island Bay, USA)
The high surface area-to-water volume ratio of coastal lagoons may increase the importance of sediment–water column interactions (Nowicki and Nixon, 1985, Sand-Jensen and Borum, 1991). Macroalgae can affect N fluxes from the sediments to the water column by intercepting regenerated N (Valiela et al., 1992, Bierzychudek et al., 1993, McGlathery et al., 1997) and may thereby limit phytoplankton growth (Thybo-Christesen et al., 1993). The algae can intercept both dissolved inorganic N (DIN) and
Case study 3 — variations in biomass distribution among benthic and pelagic producers in a tropical reservoir (Lake Brobo, West Africa)
Freshwater lakes can be highly dynamic from the standpoint of relative biomass of various autotrophs. This variability, in turn, can influence how the ecosystem responds to increased inputs of limiting nutrients.
The first freshwater case study was conducted at Lake Brobo, West Africa. This small (area=85 ha) reservoir is eutrophic (phytoplankton chlorophyll a=10–20 μg l−1) and shallow (mean depth=2.9 m), and it experiences yearly fluctuations in depth of up to 1.5 m. Secchi transparencies vary
Case study 4 — P uptake by periphyton and plankton in a shallow subtropical lake (Lake Okeechobee, USA)
As indicated in the previous case study and in a number of published reports (e.g. Sand-Jensen and Borum, 1991, Zimba, 1995, Lowe, 1996, Steinman et al., 1997), shallow lakes can sometimes support a high biomass of epiphyton and epipelon. Where this occurs, the lake's P cycle is likely to include a close coupling between the attached algae and plankton (Wetzel, 1996). A number of studies have shown that co-occurring freshwater attached algae and phytoplankton are limited by the same nutrient,
Synthesis
The dynamics of primary producer communities illustrated by the four case studies can be placed into a broader context using a conceptual model (Fig. 6). For simplicity, not all pathways are shown and consumers are not included in the model. The case studies of Hog Island Bay and Lake Okeechobee provided examples of nutrient uptake from the water or sediments by phytoplankton, epiphyton, and benthic algae (arrows 1). These autotrophs, along with vascular plants, also can release soluble
Conclusion
According to published models (Sand-Jensen and Borum, 1991, Duarte, 1995, Valiela et al., 1997a), increased loading of nutrients to freshwater and marine ecosystems can bring about a transition from vascular plant to algal dominance. Microalgae (phytoplankton and attached algae) have higher nutrient uptake rates than macroalgae, which in turn have higher rates than freshwater and marine angiosperms. With increased growth of phytoplankton and macroalgae there is a reduction in light penetration
Acknowledgements
The Hog Island Bay research was supported by The Virginia Coast Reserve LTER Project and an additional award to Karen McGlathery (National Science Foundation award numbers DEB-9411974 and DEB-9805928, respectively). The research on Waquoit Bay was supported by a National Estuarine Research Reserve Graduate Research Fellowship from the National Oceanic and Atmospheric Administration (award number NA77OR0228) and a United States Environmental Protection Agency STAR Fellowship for Graduate
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