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Primary Productivity, Chemo‐organotrophy, and Nutritional Interactions of Epiphytic Algae and Bacteria on Macrophytes in the Littoral of a Lake

Author:
Allen, Harold L.
Source:
Ecological monographs 1971 v.41 no.2 pp. 97-127
ISSN:
0012-9615
Subject:
Caulobacter, Chara, Najas flexilis, Schoenoplectus acutus, Scirpus, acetates, acidification, active transport, algae, bacteria, bacterial communities, bioassays, biomass, carbon 14, carbon dioxide, carotenoids, chlorophyll, cold, dissolved organic carbon, ecosystems, emergent plants, enzyme kinetics, epiphytes, glucose, hydrochloric acid, ice, inorganic phosphorus, iron, isotope labeling, kinetics, lakes, littoral zone, metabolites, mixed culture, photosynthesis, phytoplankton, polymethylmethacrylate, primary productivity, solutes, submerged aquatic plants, surface area, temperature, toxicity, trophic relationships, vegetation, vitamins, winter
Abstract:
Epiphytic algal and bacterial in situ community metabolism and physiological—nutritional relationships of macrophyte—epiphyte systems were investigated in the littoral zone of a small temperate lake from April 1968 through May 1969. Annual primary productivity, chemo—organotrophy of dissolved organic compounds, and field and laboratory studies of macrophyte—epiphyte interactions were monitored by carbon—14 techniques. Productivity measurements of epiphytic algae on artificial substrates colonized in emergent (Scirpus acutus Muhl.) and submergent (Najas flexilis L. and Chara spp.) macrophytic vegetation sites were compared over an annual period with pigment (corrected chlorophyll a and total plant carotenoids) estimates of biomass. Changes in biomass are not proportional to changes in photosynthetic activity, except during periods of intense productivity. The mean daily productivity of epiphytic algae was higher per unit macrophyte surface area of emergent plants (336 mg C m— ² day— ¹) than on submerged plants (258 mg C m— ² day— ¹). Mean daily productivity per unit area of the littoral zone, for all of the macrophytic surface area colonized, was 195 and 1,807 mg C m— ² day— ¹ in the Scirpus and Najas—Chara dominated sites, respectively. The total annual production by algal epiphytes in the Scirpus and Najas—Chara dominated sites was 2.86 and 35.00 g C m— ² of lake surface year— ¹, respectively. Estimates of annual net production of macrophytes and epipelic algae, derived from studies undertaken during the same time period as reported in this study, indicate that epiphytic algae were responsible for 31.3% of the total littoral production. The epiphytic algae were responsible for 21.4% of the total annual production for the whole lake when the production of the pelagial phytoplankton was added to that of the littoral communities. In comparison to the pelagial phytoplankton alone, the algal epiphytes fixed an amount of carbon equivalent to 75% of the phytoplankton production over the annual period. These results indicate that algal epiphytes on submerged macrophytes may be one of the dominant primary producers in shallow—water ecosystems and may be comparable to the phytoplankton. Deposition of ¹ ⁴C—monocarbonates during in situ productivity measurements represented 38.5—71.7% of the total intracellular fixed carbon. Acidification of ¹ ⁴C—productivity samples by rinsing with dilute hydrochloric acid (0.001 N) removed 24% of previously incorporated carbon and is not recommended as a routine procedure. Physiological interactions in macrophyte—epiphyte systems were investigated by bioassay procedure. Inorganic iron added at less than 10 mg liter — ¹, and at 100 mg liter— ¹ in combination with organic compounds of chelatory or complexing ability, stimulated photosynthesis of epiphytic algae. Bioassay experiments in which vitamins, trace metals, and inorganic phosphorus were added to algal photosynthesis. Chlorophyll a, corrected for pheopigment degradation products, and total plant carotenoid levels are among the highest standing crops reported in the literature (annual maximum of chlorophyll a = 7.3 g m— ²; plant carotenoids = 40.7 SPU m— ²). Maximum concentrations were found during winter under ice cover. Epiphytic bacterial chemo—organotrophy with glucose and acetate substrates was measured at concentrations of 11—160 mg liter— ¹ and evaluated through Michaelis—Menten enzyme kinetic analysis. First—order active transport kinetics dominated throughout the annual period. Uptake of acetate (submerged plant site, mean rate = 893 mg liter— ¹ hr— ¹ dm— ²; emergent plant site, 106 mg liter— ¹ hr— ¹ dm— ²) was greater than that of glucose (submerged plant site, 586 mg liter— ¹ hr— ¹ dm— ²; emergent plant site, 54 mg liter— ¹ hr— ¹ dm— ²). Scirpus acutus was labeled in situ during photosynthesis with natural concentrations of carbon dioxide (as ¹ ⁴C). Epiphytic uptake of ¹ ⁴C—labeled, extracellular products of macrophytic origin was determined. Extracellular release of ¹ ⁴C—labeled organic matter was followed at various depths in the littoral water column. The nature of the extracellular release and the amount of ¹ ⁴C fixed by the macrophyte and transferred into the epiphytic complex suggests nutritional interactions that may be prevalent in other macrophyte—epiphyte systems. Najas flexilis, germinated and grown under axenic conditions in a defined medium, was labeled during photosynthesis and placed into the center section of Plexiglas chambers separated by membrane filters free of organic carbon contamination. Over a 3.75—hr incubation interval, a mean of 7% of the total intracellularly fixed carbon was excreted as ¹ ⁴C—labeled dissolved organic carbon. Cultured algal and bacterial epiphytes, separately and mixed in simulated natural communities, were able to utilize these extracellular products when placed into chamber sections adjoining the labeled Najas. The amount of extracellular products utilized by the mixed algal and bacterial communities changed with time, depending on the composition of the epiphytic community. The results suggest interspecific interactions where competition for specific external metabolites or organic solutes may have existed, or where toxic extracellular products may have accumulated. Laboratory uptake of low concentrations of glucose and acetate—¹ ⁴C at 5°, 11° to 12°, and 21° to 23° C by separate and mixed cultures of algal and bacterial epiphytes showed that uptake was strongly influenced by temperature, except at low temperatures where transport and diffusion mechanisms seemed to be inactivated. A sessile bacterium, Caulobacter, however, showed a highly efficient uptake system for both substrates under cold conditions. Uptake of both substrates by mixed cultures of algae and bacteria showed that bacterial uptake of both substrates by mixed cultures of algae and bacteria showed that bacterial uptake was little influenced at low substrate concentrations by the presence of algae. Epiphytic algal uptake following kinetics of simple diffusion was, however, increased in the presence of bacteria, suggesting uptake of ¹ ⁴CO₂ previously respired by the bacteria. Macrophyte—epiphyte metabolism may be an important source of dissolved organic materials and extracellular metabolites and thus may help to sustain high levels of primary productivity and chemo—organotrophy in lakes.
Agid:
5182625