Additional Abstracts .... Nixon, Scott Walker, Nan O'Donnell, James Hamilton, Peter Roman, Mike Hitchcock, Gary Rabalais, Nancy Mestas-Nunez, Alberto Report #19 Table of Contents

Louis Legendre
Department de Biologie
Universite Laval, Quebec QC G1K 7P4, Canada

The present discussion concentrates on the role of nutrients in the bottom-up control of pelagic food webs, and it considers the grazing of phytoplankton by zooplankton as the primary top-down control. Three aspects are examined: quantity of the limiting nutrient, chemical composition of nutrients, i.e. ratios of certain elements, and frequency or steadiness of nutrient inputs.

The quantity of the limiting nutrient, together with irradiance and water temperature, controls the rate of photosynthesis, i.e. phytoplankton production per unit biomass; when production is low, phytoplankton are generally small (<5 µm; picoplanktonic cyanobacteria, µ-flagellates), so that there is generally low transfer of biogenic carbon (BC) to large pelagic animals (except when there is package of small particles into large ones by large microphagous zooplankton, i.e. salps, doliolids, appendicularians, pteropods; Fortier et al. 1994); when production is high, there is either potentially high BC transfer to large animals, or massive sinking to depth of ungrazed cells.

The taxonomic composition of the phytoplankton assemblage is a major factor that determines the structure and functioning of pelagic food webs. It largely (but not solely) depends on the chemical composition of nutrients, i.e. the ratios of some elements. When there is low Si vs. N and P, diatoms are often replaced by non-Si taxa, e.g. dinoflagellates, prymnesiophytes, and picoplanktonic cyanobacteria; when there is low Si and high N vs. P, dinoflagellates and prymnesiophytes are often favored; when there is low Si and high P vs. N, there may be blooms of N₂-fixing filamentous, heterocystous cyanobacteria, which are then not limited by either N or P. It follows that: the chemical composition of nutrients may determine the sizes and edibility of phytoplankton; because small phytoplankton are grazed by microzooplankton, whose generation times are similar to those of small cells, there is tight coupling between primary production and grazing (no blooms), but generally low transfer of biogenic carbon to large pelagic animals; inedible large phytoplankton sink to depth as aggregated ungrazed cells; edible large phytoplankton potentially lead to high BC transfer to large animals.

The level of phytoplankton production and the taxonomic composition of phytoplankton (previous two paragraphs) are necessary but not sufficient conditions to ensure high BC transfer to large pelagic animals: because phytoplankton assemblages are generally not long-lasting, they influence food webs only if their time scales match those of the zooplankton grazers; ephemeral blooms of large phytoplankton may be either grazed or sink to depth, according to their taxonomic composition (edible taxa or not) and the presence or not of opportunistic grazers, but they generally have no lasting effects on the heterotrophic components of food webs. Because the generation times of microzooplankton are similar to those of small phytoplankton, the present paragraph mostly concerns large phytoplankton and their mesozooplankton grazers. Concerning the frequency or steadiness of nutrient inputs, when these are steady or high-frequency, the production characteristics of large phytoplankton match the generation times of large grazers (i.e. from weeks to months); when the inputs are low-frequency, the production characteristics of large phytoplankton may match the seasonal or annual patterns of grazers; when the inputs are irregular and/or short-lived, there is low matching, so that ungrazed blooms of large phytoplankton are often followed by massive sinking to depth of ungrazed cells.

Legendre & Rassoulzadegan (1995) proposed that the various trophic pathways in the pelagic environment are part of a continuum. They divided the continuum into four pathways: the microbial loop is an almost closed system of heterotrophic bacteria and zooflagellate grazers, in which the grazers release dissolved organic matter used as substrate by bacteria; the microbial food web has the same components as the microbial loop, plus small phytoplankton, so that there is possible BC export toward large metazoans (the expressions "microbial loop" and "microbial food web" are often confounded in the literature); in the multivorous food web, the herbivorous and microbial trophic modes both play significant roles; the herbivorous food web is dominated by large phytoplankton and herbivorous grazing.

The three aspects of nutrients discussed above are involved in the control of food webs, an alternative BC pathway being the sinking to depth of ungrazed phytoplankton. The information concerning these effects is summarized here in an IDENTIFICATION KEY:

1. Quantity of Nutrients:
   • Low: small phytoplankton, leading to the microbial food web or the microbial loop
   • Intermediate and High: large phytoplankton, see 2

2. Large Phytoplankton: Effects of the chemical composition of nutrients
   • High Si:N and Si:P: diatoms, see 3
   • Low Si:N and high N:P: dinoflagellates
     • Edible taxa, see 3
     • Inedible taxa: blooms, followed by sinking to depth of ungrazed phytoplankton
   • Low Si:N and high P:N: sometimes blooms of inedible N₂-fixing filamentous cyanobacteria, leading to the sinking to depth of ungrazed cells

3. Large Edible Phytoplankton: Effects of the frequency of nutrient inputs
   • Match the characteristics of zooplankton grazers
     • High nutrient flux, high Si:N and Si:P: diatom-based herbivorous food web
     • High nutrient flux, low Si:N and Si:P: dinoflagellate-based herbivorous food web
     • Intermediate nutrient flux: diatom- or dinoflagellate-based multivorous food web
   • Mismatch: blooms, followed by sinking to depth of ungrazed phytoplankton

The anthropogenic inputs of nutrient in coastal waters may affect the three aspects of nutrients discussed above, resulting in harmful algal blooms (HABs; several ideas below are from Paerl 1997). Increases in the overall quantity of nutrients enhance phytoplankton production, which may be transferred or not to large pelagic animals; in vertically stratified shallow waters, the massive sinking to the bottom of ungrazed phytoplankton increases the biological oxygen demand, leading to hypoxia (reduction of oxygen concentrations) and sometimes anoxia (depletion of oxygen). Changes in the chemical composition of nutrients may have different effects: low Si:N and Si:P generally promote the growth of taxa other than diatoms, some of these not leading to food webs that support large pelagic animals; P loading is presently low, but there is episodic release in the water column of P accumulated in sediments, causing HABs of toxic N₂-fixing filamentous, heterocystous cyanobacteria; high anthropogenic N inputs in coastal and continentally bound seas in the Northern Hemisphere generally correspond to the main HAB areas. Concerning changes in the frequency of inputs, continuous inputs may favor the establishment of new, stable food webs if the phytoplankton taxa are edible, whereas irregular and/or short-lived inputs increase the likelihood of massive sinking to the bottom of ungrazed phytoplankton.

References

Fortier, L., J. le Fevre and L. Legendre. 1994. Export of biogenic carbon to fish and to the deep ocean: the role of large planktonic microphages. J. Plankton Res. 16: 809-839.

Legendre, L. & F. Rassoulzadegan. 1995. Plankton and nutrient dynamics in marine waters. Ophelia 41: 153-172.

Paerl, H.W. 1997. Coastal eutrophication and harmful algal blooms: Importance of atmospheric deposition and groundwater as "new" nitrogen and other nutrient sources. Limnol.Oceanogr. 42: 1154-1165.