Complex interactions between autotrophs in shallow marine and freshwater ecosystems: implications for community responses to nutrient stress

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Abstract

The relative biomass of autotrophs (vascular plants, macroalgae, microphytobenthos, phytoplankton) in shallow aquatic ecosystems is thought to be controlled by nutrient inputs and underwater irradiance. Widely accepted conceptual models indicate that this is the case both in marine and freshwater systems. In this paper we examine four case studies and test whether these models generally apply. We also identify other complex interactions among the autotrophs that may influence ecosystem response to cultural eutrophication. The marine case studies focus on macroalgae and its interactions with sediments and vascular plants. The freshwater case studies focus on interactions between phytoplankton, epiphyton, and benthic microalgae. In Waquoit Bay, MA (estuary), controlled experiments documented that blooms of macroalgae were responsible for the loss of eelgrass beds at nutrient-enriched locations. Macroalgae covered eelgrass and reduced irradiance to the extent that the plants could not maintain net growth. In Hog Island Bay, VA (estuary), a dense lawn of macroalgae covered the bottom sediments. There was reduced sediment–water nitrogen exchange when the algae were actively growing and high nitrogen release during algal senescence. In Lakes Brobo (West Africa) and Okeechobee (FL), there were dramatic seasonal changes in the biomass and phosphorus content of planktonic versus attached algae, and these changes were coupled with changes in water level and abiotic turbidity. Deeper water and/or greater turbidity favored dominance by phytoplankton. In Lake Brobo there also was evidence that phytoplankton growth was stimulated following a die-off of vascular plants. The case studies from Waquoit Bay and Lake Okeechobee support conceptual models of succession from vascular plants to benthic algae to phytoplankton along gradients of increasing nutrients and decreasing underwater irradiance. The case studies from Hog Island Bay and Lake Brobo illustrate additional effects (modified sediment–water nutrient fluxes, allelopathy or nutrient release during plant senescence) that could play a role in ecosystem response 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

References (83)

  • D.I. Taylor et al.

    Responses of coastal lagoon plant communities to different forms of nutrient enrichment — a mesocosm experiment

    Aquatic Botany

    (1995)
  • R.G. Wetzel

    Benthic algae and nutrient cycling in lentic freshwater ecosystems

  • J. Barica

    Collapses of Aphanizomenon flos-aquae blooms resulting in massive fish kills in eutrophic lakeseffect of weather

    Verhandlungen der Internationale Vereinigung fur Theoretische und Angewandte Limnologie

    (1978)
  • L.E. Barnese et al.

    Effects of nitrogen, phosphorus and carbon enrichment on planktonic and periphytic algae in a softwater, oligotrophic lake in Florida, USA

    Hydrobiologia

    (1994)
  • D.E. Barshaw et al.

    A long-term study on the behavior and survival of early juvenile American lobster, (Homarus americanus), in three naturalistic substrateseelgrass, mud, and rocks

    Fishery Bulletin

    (1988)
  • C. Berger

    In situ primary production, biomass, and light regime in the Wolderwijd, the most stable Oscillatoria agardhii lake in the Netherlands

    Hydrobiologia

    (1989)
  • A. Bierzychudek et al.

    Effects of macroalgae, night and day, on ammonium profiles in Waquoit Bay

    Biological Bulletin

    (1993)
  • S.C. Blumenshine et al.

    Benthic-pelagic linksresponses of benthos to water-column nutrient enrichment

    Journal of the North American Benthological Society

    (1997)
  • M. Bricelj et al.

    Predatory risk of juvenile bay scallops, Argopecten irradians in eelgrass habitat

    Journal of Shellfish Research

    (1991)
  • D.A. Bronk et al.

    Nitrogen uptake, dissolved organic nitrogen release, and new production

    Science

    (1994)
  • R. Buchsbaum et al.

    Available and refractory nitrogen in detritus of coastal vascular plants and macroalgae

    Marine Ecology Progress Series

    (1991)
  • D.J. Burdige et al.

    The biogeochemical cycling of dissolved organic nitrogen in estuarine sediments

    Limnology and Oceanography

    (1998)
  • J.M. Burkholder et al.

    Pfiesteria piscidida and other Pfiesteria like dinoflagellates: behavior, impacts, and environmental controls

    Limnology and Oceanography

    (1997)
  • S.R. Carpenter et al.

    Cascading trophic interactions and lake productivity

    BioScience

    (1985)
  • S.R. Carpenter et al.

    Management of eutrophication in lakes subject to potentially irreversible change

    Ecological Applications

    (2000)
  • S.R. Carpenter et al.

    Regulation of lake primary productivity by food web structure

    Ecology

    (1987)
  • J.L. Confer

    Interrelations among plankton, attached algae, and the phosphorus cycle in artificial open systems

    Ecological Monographs

    (1974)
  • S.R. Cornell et al.

    Atmospheric inputs of dissolved organic nitrogen to the oceans

    Nature

    (1995)
  • Costa, J.E., 1988. Distribution, production, and historical changes in abundance of eelgrass (Zostera marina) in...
  • W.C. Dennison et al.

    Photosynthetic response of Zostera marina L. (eelgrass) to in situ manipulations of light intensity

    Oecologia

    (1982)
  • J.A. Downing

    Marine nitrogen:phosphorus stoichiometry and the global N:P cycle

    Biogeochemistry

    (1997)
  • C. Duarte

    Submerged aquatic vegetation in relation to different nutrient regimes

    Ophelia

    (1995)
  • S. Enriquez et al.

    Patterns of decomposition rates among photosynthetic organismsimportance of detritus C:N:P content

    Oecologia

    (1993)
  • V. Gotceitas et al.

    Use of eelgrass beds (Zostera marina) by juvenile Atlantic cod (Gadus morhua)

    Canadian Journal of Fisheries and Aquatic Sciences

    (1997)
  • L.A. Hansson

    Quantifying the impact of periphytic algae on nutrient availability for phytoplankton

    Freshwater Biology

    (1990)
  • J. Hauxwell et al.

    Macro-algal canopies associated with increased anthropogenic nitrogen supply contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems

    Ecology

    (2000)
  • K.E. Havens et al.

    Phosphorus cycling among lake plankton and periphyton: relationship to irradiance and phosphate availability

    Archiv für Hydrobiologie

    (2000)
  • K.E. Havens et al.

    Rapid ecological changes in a large subtropical lake undergoing cultural eutrophication

    Ambio

    (1996)
  • K.E. Havens et al.

    Light availability as a possible regulator of cyanobacteria species composition in a shallow subtropical lake

    Freshwater Biology

    (1998)
  • M.E. Hay et al.

    Marine plant–herbivore interactionsthe ecology of chemical defense

    Annual Review of Ecology and Systematics

    (1988)
  • K.L. Heck et al.

    Fishes and decapod crustaceans of Cape Cod eelgrass meadowsspecies composition, seasonal abundance patterns and comparison with unvegetated substrates

    Estuaries

    (1989)
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