The importance of considering biological processes when setting total maximum daily loads (TMDL) for phosphorus in shallow lakes and reservoirs.

Total maximum daily loads (TMDL) are required by the US Environmental Protection Agency for pollutants that have impaired the designated uses of surface waters in the nation. Setting an appropriate TMDL requires quantitative information on both the external pollutant inputs and the processes affecting pollutant dynamics within the ecosystem. Here we focus on phosphorus (P), a globally important pollutant of freshwater lakes. We consider how biological processes (including those related to algae, plants, invertebrates and fish) can influence the ability of lakes to assimilate P, and in turn the ability of managers to select appropriate TMDLs. The primary focus is on shallow eutrophic lakes, with Lake Okeechobee (Florida, USA) serving as a case study. The paper deals only with in-lake processes as they relate to setting the TMDL and not the subsequent issue of load allocation among pollution sources. The results indicate that the ability of a shallow lake to assimilate P is substantially reduced when surplus levels of P occur in the water column, the phytoplankton becomes dominated by cyanobacteria, the benthic invertebrate community becomes dominated by oligochaetes, and submerged plant biomass is low. If some of these biological changes can be reversed in a rehabilitation program then the lake may be able to support a higher TMDL.

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

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 under-water 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.

Nutrient dynamics and the eutrophication of shallow lakes Kasumigaura (Japan), Donghu (PR China), and Okeechobee (USA).

We compared the nutrient dynamics of three lakes that have been heavily influenced by point and non-point source pollution and other human activities. The lakes, located in Japan (Lake Kasumigaura), People's Republic of China (Lake Donghu), and the USA (Lake Okeechobee), all are relatively large (> 30 km2), very shallow (< 4 m mean depth), and eutrophic. In all three lakes we found strong interactions among the sediments, water column, and human activities. Important processes affecting nutrient dynamics included nitrogen fixation, light limitation due to resuspended sediments, and intense grazing on algae by cultured fish. As a result of these complex interactions, simple empirical models developed to predict in-lake responses of total phosphorus and algal biomass to external nutrient loads must be used with caution. While published models may provide 'good' results, in terms of model output matching actual data, this may not be due to accurate representation of lake processes in the models. The variable nutrient dynamics that we observed among the three study lakes appears to be typical for shallow lake systems. This indicates that a greater reliance on lake-specific research may be required for effective management, and a lesser role of inter-lake generalization than is possible for deeper, dimictic lake systems. Furthermore, accurate predictions of management impacts in shallow eutrophic lakes may require the use of relatively complex deterministic modeling tools.

Modeling water resources: have we got it right?

Aquatic scientists generally recognize that controlled experiments are required to establish cause-effect relationships (e.g., Havens and Aumen, 2000), and understanding ecological processes is key to accurately predicting complex ecosystem responses. However, resource managers may have at their disposal only a limited amount of observational data when faced with management decisions. Hence, there may be a tendency to use simple empirical models for decision making. An example of eutrophication management in lakes illustrates a pitfall of this approach when used independently of other scientific information.

Hurricane effects on a shallow lake ecosystem and its response to a controlled manipulation of water level.

In order to reverse the damage to aquatic plant communities caused by multiple years of high water levels in Lake Okeechobee, Florida (U.S.), the Governing Board of the South Florida Water Management District (SFWMD) authorized a "managed recession" to substantially lower the surface elevation of the lake in spring 2000. The operation was intended to achieve lower water levels for at least 8 weeks during the summer growing season, and was predicted to result in a large-scale recovery of submerged vascular plants. We treated this operation as a whole ecosystem experiment, and assessed ecological responses using data from an existing network of water quality and submerged plant monitoring sites. As a result of large-scale discharges of water from the lake, coupled with losses to evaporation and to water supply deliveries to agriculture and other regional users, the lake surface elevation receded by approximately 1 m between April and June. Water depths in shoreline areas that historically supported submerged plant communities declined from near 1.5 m to below 0.5 m. Low water levels persisted for the entire summer. Despite shallow depths, the initial response (in June 2000) of submerged plants was very limited and water remained highly turbid (due at first to abiotic seston and later to phytoplankton blooms). Turbidity decreased in July and the biomass of plants increased. However, submerged plant biomass did not exceed levels observed during summer 1999 (when water depths were greater) until August. Furthermore, a vascular plant-dominated assemblage (Vallisneria, Potamogeton, and Hydrilla) that occurred in 1999 was replaced with a community of nearly 98% Chara spp. (a macro-alga) in 2000. Hence, the lake"s submerged plant community appeared to revert to an earlier successional stage despite what appeared to be better conditions for growth. To explain this unexpected response, we evaluated the impacts that Hurricane Irene may have had on the lake in the previous autumn. In mid-October 1999, this category 1 hurricane passed just to the south of the lake, with wind velocities over the lake surface reaching 90 km h(-1) at their peak. Output from a three-dimensional hydrodynamic/sediment transport model indicates that during the storm, current velocities in surface waters of the lake increased from near 5 cm s(-1) to as high as 100 cm s(-1). These strong velocities were associated with large-scale uplifting and horizontal transport of fine- grained sediments from the lake bottom. Water quality data collected after the storm confirmed that the hurricane resulted in lake-wide nutrient and suspended solids concentrations far in excess of those previously documented for a 10-year data set. These conditions persisted through the winter months and may have negatively impacted plants that remained in the lake at the end of the 1999 growing season. The results demonstrate that in shallow lakes, unpredictable external forces, such as hurricanes, can play a major role in ecosystem dynamics. In regions where these events are common (e.g., the tropics and subtropics), consideration should be given to how they might affect long-term lake management programs.

Complex analyses of plankton structure and function.

This paper critically evaluates some complex methods that have been used to characterize the structure and function of freshwater plankton communities. The focus is on methods related to plankton size structure and carbon transfer. The specific methods reviewed are 1) size spectrum analysis, 2) size-fractionated phytoplankton productivity, 3) size-fractionated zooplankton grazing, 4) plankton ecological transfer efficiency, and 5) grazer effects on phytoplankton community structure. Taken together, these methods can provide information on community ecological properties that are directly related to practical issues including water quality and fisheries productivity. However, caution is warranted since application without a complete understanding of assumptions and context of the manipulations could lead to erroneous conclusions. As an example, experimental studies involving the addition or removal of zooplankton, especially when coupled with nutrient addition treatments, could provide information on the degree of consumer vs. resource control of phytoplankton. Resource managers subsequently could use this information in developing effective measures for controlling nuisance algal biomass. However, the experiments must be done critically and with sufficient safeguards and other measurements to ensure that treatments (e.g., zooplankton exclosure by screening of water) actually are successful and do not introduce other changes in the community (e.g., removal of large algae). In all of the methods described here, the investigator must take care when generalizing results and, in particular, carry out a sufficient number of replications to encompass both the major seasonal and spatial variation that occurs in the ecosystem.

Secondary nitrogen limitation in a subtropical lake impacted by non-point source agricultural pollution.

A 20-year history of nutrient limitation was quantified for Lake Okeechobee, a nutrient-impacted lake in Florida, USA. Limiting status (nitrogen versus phosphorus) was estimated from deviations between trophic state index (TSI) parameters, calculated from routine monitoring data. The lake is presently nitrogen-limited. However, historical trends in the TSI deviations indicate that contemporary nitrogen limitation is a secondary, unnatural condition that has arisen due to excessive phosphorus loading. Prior to 1980, there was evidence of lake-wide limitation by phosphorus, rather than nitrogen. The finding of secondary nitrogen limitation in Lake Okeechobee has important management implications. Phosphorus loads are presently being reduced in order to reduce in-lake concentrations and create phosphorus-limited conditions (nitrogen limitation is undersirable because it has favored bloom-forming cyanobacteria). The present results indicate that this long-term management goal is ecologically sound; it is consistent with the concept of restoration of the lake.

Structural and functional responses of a freshwater plankton community to acute copper stress.

An in-situ experiment was performed to quantify the impacts of copper sulfate on plankton structure and carbon dynamics. Plankton were exposed to 140 microg litre(-1) copper in quadruplicate mesocosms. Community structure was monitored for 14 days by microscopical counts and compared with untreated controls. Carbon dynamics were assessed by tracer studies using (14)C bicarbonate and (14)C glucose, to follow the fate of carbon in the algal- and bacterial-based pathways, respectively. Copper reduced the dry-weight biomass of zooplankton, ciliates, flagellates, and autotrophic phytoplankton. Bacterial biomass was increased by an order of magnitude relative to the controls. The bacterial response was most likely due to reduced grazing pressure and/or nutrient release from dying plankton. Copper reduced the effectiveness of the food web in transporting carbon to the surviving zooplankton. Bacterial-based pathways were more greatly affected than algal-based pathways, because zooplankton in the copper treatment were macro-grazers (cyclopoids), which cannot utilize bacteria.

An experimental comparison of the effects of two chemical stressors on a freshwater zooplankton assemblage.

Mesocosms in an Ohio, USA lake were dosed with ten levels (0-100 microg liter(-1)) of copper (experiment 1) or Carbaryl (experiment 2). Zooplankton responses were determined after 4-day incubations. Species level responses differed for the two chemicals; community level responses were very similar. Across the gradients of increasing Cu or Carbaryl doses, cladocerans were greatly reduced and copepods became dominant. For Carbaryl, the response was consistent with that reported previously. For Cu, different responses were previously observed at other lakes. The taxonomic composition of the zooplankton may largely determine the community level response. In the present experiments, cladoceran declines may have secondarily affected food web function. In the Carbaryl experiment, where the chemical did not directly suppress algae, their biomass increased with dose level. This coincided with the cladoceran decline, suggesting an algal response to reduced top-down control.

Zooplankton community responses to chemical stressors: a comparison of results from acidification and pesticide contamination research.

The response of freshwater zooplankton communities to two chemical stressors, acidification and pesticide contamination, were investigated in a review of published research results. The objective was to test Odum's predictions (Odum, 1985) that in response to stress, both the average body size of organisms and their efficiency in utilizing resources are reduced. Acidification and pesticide contamination were both found to favor dominance by small cladorecans and rotifers, the smallest zooplankton taxa. This finding was consistent with Odum's predictions, however, there were exceptions to the trend. The dominance of small taxa may be due to rapid reproductive rates, physiological tolerance, development with few transitions through sensitive stages (eg. post-molting), or to the great richness of small species. Regardless of the mechanism, there is evidence that when acidification and pesticide contamination result in small zooplankton dominance, the efficiency of carbon and energy transfer from algae to zooplankton is reduced. This finding is also consistent with Odum's predictions.

Acid and aluminum effects on the survival of littoral macro-invertebrates during acute bioassays.

Six common macro-invertebrates were exposed to soft water at pH 4.5, with or without 200 microg liter(-1) Al added. Survivals were determined at 6, 12, 24 and 48 h and compared with neutral pH, Al-free controls. The order of acid-sensitivity among the test animals, from greatest to least (with mean 24/48 h survivals in the pH 4.5, low Al treatment in parentheses), was: Caenis sp. (2%) > Hyalella azteca (12%) > Enallagma sp. (20%) > Gyraulus sp. (55%) > Chironomidae (94%) > Hydracarina (99%). Aluminum significantly reduced the survivals of Gyraulus, Hyalella and Chironomidae. The latter group experienced no significant mortality at pH 4.5 except when Al was present. In contrast, the Hydracarina were unaffected by both acid and acid plus Al exposure, and the survivals of Enallagma and Caenis at low pH were enhanced by Al. These differential responses to the treatments indicate that both acid and Al stress may control the structure of the littoral macroinvertebrate community in acid lakes.

Littoral zooplankton responses to acid and aluminum stress during short-term laboratory bioassays.

During autumn 1990, littoral zooplankton were collected from three alkaline lakes in Ohio, USA. Toxicity tests were performed, in which animals were placed into treatments of pH 4.5, with or without 500 microg litre(-1) Al added. Percentage survival after 24 h was determined for each test species, and compared to survival in controls (pH roughly 8.0). Three distinct responses were observed: (1) Four cladocerans, Simocephalus serrulatus, Diaphanosoma birgii, Acantholeberis curvirostris and Chydorus sphaericus, were tolerant of both acid and Al, with no significant reductions in survival in the treatments. (2) The cladoceran Eurycercus lamellatus and the capepod Acanthocyclops vernalis were sensitive to both acid and Al, and suffered 100% mortality in both treatments. (3) The cladocerans Camptocercus rectirostris, Alona costata and Pleuroxus denticulatus, and the copopod Mesocyclops edax showed decreased survival in the acid treatment, and a significantly greater decrease in the acid plus Al treatment. For nine of the ten test species, the results were consistent with previous survey and paleolimnological studies. The results indicate that direct toxic effects of H+ and Al ions largely determine the responses of these common littoral species to acidification.

Phytoplankton succession during acidification with and without increasing aluminum levels.

An in situ mesocosm experiment was performed to investigate the role of aluminum in controlling phytoplankton community succession during lake acidification. Large (2000 liter) mesocosms were suspended in mesotrophic East Twin Lake, Ohio, USA. Duplicates were either untreated controls (pH 8.8), acidified to pH 4.5 over 23 days, or acidified and spiked with 200 microg/liter Al in incremental additions. Filamentous blue greens, diatoms and other chrysophytes became extinct in both acid treatments, but declined most rapidly where Al levels were also increased. The large desmid Closterium and the filamentous chlorophyte Mougoetia became dominant in the Acid treatment. In the Acid + Al treatment, these algae also became dominant, but the species with greatest biomass was the dinoflagellate Peridinium inconspicuum. Acidification (with or without added Al) also resulted in a significant shift in the algal size spectrum to larger (> 20 microm) cells.

Aluminum binding to ion exchange sites in acid-sensitive versus acid-tolerant cladocerans.

Two acid-sensitive cladocerans, Daphnia galeata mendotae and D. retrocurva, and one acid-tolerant one, Bosmina longirostris, were exposed for 24 h to pH 5.0 and 200 microg liter(-1) total Al. The entire procedure was replicated on three dates in summer 1989. Mortality rates were determined, and the extent of Al binding to ion exchange sites determined using hematoxylin staining. Both daphnids consistently experienced near 100% mortalities, while mortalities for B. longirostris were always near zero. The daphnids showed marked Al binding at the maxillary glands, the site of ion exchange, while B. longirostris showed no noticeable Al binding.

Acid and aluminum effects on freshwater zooplankton: an in situ Mesocosm study.

An in situ mesocosm experiment was performed to evaluate the role of aluminum toxicity in determining zooplankton community responses to take acidification. Large plastic enclosures were suspended in East Twin Lake, Ohio, USA, and duplicates were either untreated controls (pH 8.8), acidified to pH 4.5 over a 23 day period, or acidified and also spiked with incremental additions of Al, to produce a final inorganic monomeric Al level of 180 microg/liter at pH 4.5. Zooplankton abundance and species richness declined in both acid treatments, relative to the control, as numerous acid-sensitive species were eliminated. All of the acid-sensitive species were also Al-sensitive, declining in abundance more rapidly in the acid plus Al treatment than in the acid-alone treatment. Only two small cladocerans (Bosmina longirostris and Chydorus sphaericus) were acid tolerant. Both were also tolerant of elevated Al levels.