Linkages between chemical and physical responses and biological populations

Transcription

1 Section 3 Linkages between chemical and physical responses and biological populations Limnol. Oceanogr., 41(5), 1996, , by the American Society of Limnology and Oceanography, Inc. Annual cycle of autotrophic and heterotrophic production in a small, monomictic Piedmont lake (Lake Oglethorpe): Analog for the effects of climatic warming on dimictic lakes Karen G. Porter and Patricia A. Saunders Institute of Ecology, University of Georgia, Athens Kurt A. Haberyan Department of Biology, Northwest Missouri State University, Maryville Alexander E. Macubbin Department of Experimental Therapeutics, Roswell Park Cancer Institute, Buffalo, New York Timothy R. Jacobsen Cumberland County College, Vinelands, New Jersey Robert E. Hodson School of Marine Sciences, University of Georgia, Athens Abstract Lake Oglethorpe, Georgia, is a small, monomictic impoundment in the southeastern U.S. Piedmont region. Seasonal differences in ecological processes correspond to the two major stratification patterns and result in seasonal differences in pelagic community structure,. The winter mixed period (November-March) provides light and temperatures suitable for active nutrient regeneration and uptake, population growth of edible phytoplankton and crustacean zooplankton, and low bacterial abundance and production. Monthly estimates of daily primary productivity are in the mesoeutrophic range (40-l,420 mg C m-2 d-l); however, mean annual primary productivity is in the eutrophic range (500 mg C m-2 yr-i) because of greater activity in winter and an extended growing season. The stratified period (April-October) is characterized by rapid development of hypolimnetic anoxia, high bacterial production, cyanobacteria and large algae, heterotrophic flagellates, ciliates, rotifers, small cyclopoid copepods, and Chaoborus. Heterotrophic activity, HPLC chlorophyll a, and grazer activity were highest at the epilimnetic-metalimnetic boundary. Bacterial abundances ( x 1 O6 cells ml- I) increased in the hypolimnion during the stratified period. Long-term (1978-l 994) warming within the water column ( O. 10 C yr-i) follows midwinter (January) air temperature trends. Using Lake Oglethorpe as an analog, we predict as consequences of climatic warming in northern dimictic lakes: increases in nutrient cycling rates, winter primary and secondary productivity, summer heterotrophic production, and microbial components of the food web,. Acknowledgments In addition to the authors, Adrieen Debiase, Yvette Feig, Hal King, Doug Leeper, Bob McDonough, Judy Meyer, Michael Pace, John Orcutt, Amy Parker, Bob Sanders, and Susan Bennett Wilde provided major assistance in data collection, analysis and interpretation. John Chick and Phil Dixon aided in statistical analysis of the long-term thermal data, and Rob Reinert, David Bruce, and Mike Van Den Avyle provided insights about fish assemblages. Thanks to the Helfmeyers for access to Lake Oglethorpe from their property. This research was supported indirectly by several grants from the National Science Foundation. Contribution 49 of the Lake Oglethorpe Limnological Association. 1041

2 1042 Porter et al. Most small natural lakes in North America are glacial in origin and are classified as temperate and dimictic (Hutchinson 1957). Studies of these north-temperate lakes are the basis for many limnological paradigms. Comparable small water bodies below the southern extent of dimixis (36 N in the Midwest, 40 N in the Northwest, and 38 N in the Southeast, Hutchinson 1957) are generally warm monomictic impoundments and have received relatively little study. Limnological comparisons have been made among tropical and temperate lakes but rarely include those at intermediate latitudes (e.g. Lewis 1987). Most reviews considering lentic systems of southeastern North America focus on natural lakes, which occur primarily on the Coastal Plain (Frey 1963; Crisman 1992), farm ponds (Menzel and Cooper 1992), and large reservoirs (Soballe et al. 1992). A recent EPA study of small (~648 ha), stratifying impoundments in the Piedmont of North Carolina, South Carolina, and Georgia provides the first comparative survey of these systems (Raschke 1993, 1994). Lake Oglethorpe, our study site, was included in the EPA survey and is considered typical of small impoundments in the region with lakelike characteristics, being deep enough to stratify and having a relatively long water residence time. We define a small lake as any standing body of water, natural or anthropogenic, that is lo-500 ha in surface area, deep enough to stratify, and with a long mean water residence time (> 2 months). Small monomictic impoundments are the appropriate systems to compare and contrast with small dimictic lakes of the north-temperate zone. Monomictic lakes may also be good analogs for the changes that could occur in dimictic lakes due to climatic warming. In Canadian Shield lakes, regional warming trends have resulted in an increase in ice-free period and winter phytoplankton biomass (Schindler et al. 1990). If warming trends continue, the thermal regimes of many small dimictic lakes may become more like those in warm monomictic systems (i.e. lacking a winter stratification period and with warmer water temperatures year-round). A better understanding of limnological processes in warm monomictic lakes such as Lake Oglethorpe may improve predictions of the effects of climatic warming in northern lakes. Our purpose is to provide a conceptual model of a monomictic lake in the southeastern Piedmont by describing ecological processes and associations over an annual cycle in Lake Oglethorpc, Georgia. In order to characterize seasonal differences, we present a 13-month study of physical and chemical patterns and of autotrophic and heterotrophic processes during 1978-l 979. Our discussion of physical and chemical patterns includes examination of temperature and dissolved oxygen measurements spanning a 16.5-yr period. An annual cycle of organic sedimentation is provided for 1983-l 984. We summarize studies of specific aspects of microbial production and consumption. These provide a general description of seasonal shifts in the relative importance of autotrophic and heterotrophic production to food-web structure that correspond to the two major patterns of thermal regime: mixis and stratification. Finally, we use these thermally driven ecological patterns to predict the effects of climatic warming on dimictic lakes in north-temperate regions. Methods Study site-lake Oglethorpe is in Oglethorpe County ( N, W) and has been a study site for researchers at the nearby University of Georgia, Athens, since This small (AO = 30 ha) impoundment was created in It has a maximum depth of 8.7 m, a mean depth of 2.3 m, and a mean hydraulic residence time of 80 d (Raschke 1993). Compared with other small impoundments in the southeastern Piedmont, Lake Oglethorpe is characterized as mesotrophic by the EPA because of moderate epilimnetic nutrient (24 pg liter-* mean total P) and chlorophyll a concentrations (10 pg liter-l mean Chl a) and a Carlson trophic state index of 53 during summer stratified period (Raschke 1994, pers. comm.). The watershed consists of forests, farmlands, and private residences. The red-brown color associated with clay loading has been observed in the lake, but in recent years these events have been rare and have apparently declined as watershed development-a major cause of clay loading in the Piedmont (Mulholland and Lenat 1992)-has leveled off. The lake is used primarily for recreation, particularly fishing and swimming. The fish assemblage in both 1977 and 1993 included bluegill (Lepomis machrochirus), green sunfish (Lepomis cyanellus), redbreast (Lepomis auritus), black crappie (Pomoxis nigromaculatus), golden shiner (Notemigonis crysoleucus), and largemouth bass (Micropterus salmoides; Orcutt 1982; D. Bruce unpubl. data). Sampling and analyses -In 1979, monthly midday sampling was done at a permanent deep-water, foredam station at l-m depth intervals (down to 7 m). Temperature and dissolved oxygen profiles were measured with an in situ thermistor and dissolved oxygen electrode (YSI Model 57). To look for possible long-term trends, we examined temperature profiles collected at irregular intervals over a 17-yr period (1978-l 994). Although a large data set has been accumulated (N = 303 dates with temperature profiles), profiles were not obtained at consistent time intervals. Therefore, we calculated detrended monthly means (N = 108) for measurements of temperature from each discrete depth (l-m intervals to 7-m depth) and the water-column average. Data were entered into general linear models procedure (SAS, version 6) using month and year as independent variables and month as a class variable. Patterns in air temperature and rainfall data for the area (NCDC ) were similarly assessed (SAS, version 6). Light profiles were measured at 0.25-m intervals with a LiCor LI-188B PAR irradiance meter. Extinction coefficients were calculated according to Wetzel and Likens (1979). Whole-water samples were collected at l-m depth intervals with an g-liter PVC Van Dorn bottle. Subsamples were processed and analyzed for concentrations of soluble reactive P (SRP) and total P (TP) (Menzel and Corwin

3 Monomictic Lake Oglethorpe ; Murphy and Riley 1962), ammonia N (Solorzano 1969), and nitrate and nitrite (Strickland and Parsons 1972). Dissolved inorganic and organic C (DIC and DOC) were measured by infrared gas analysis (Menzel and Vaccare 1964). HPLC chlorophyll a was determined (Jacobsen 1982). Primary production was determined by the 14C method (Schindler et al. 1972) using midmorning in situ incubations at l-m intervals from the surface to the 7-m depth. Lugol s iodine-preserved phytoplankton were counted by the Utermohl method (Porter 1973). Samples for protozoan, rotifer, and crustacean zooplankton enumeration were obtained on these same sample trips, and these methods are reported elsewhere (Orcutt and Pace 1984; Pace and Orcutt 1981; Pace 1982). Bacteria were enumerated by the DAPI direct count method (Porter and Feig 1980). Heterotrophic potential - the maximal uptake and mineralization of [ 14C] glucose (Vmax)-was measured throughout to assess patterns of bacterial production (Wright and Hobbie 1966; Vaccaro et al. 1977). Particulate adenosine triphosphate (ATP) concentrations were determined (Wiebe and Bancroft 1975). In 1983-l 984, organic sedimentation was measured monthly with replicated (N = 8) sediment traps suspended at 2, 4, and 6 m in the water column. Traps consisted of 49-mm-diameter, 350-mm-long PVC tubes attached to the circumference of a 0.5-m-diameter frame. Saturated saline solution was used to exclude detritivores from screwtop powder jars threaded to the bottom of each tube. Total and ash-free dry weights were determined for contents of jars collected at monthly intervals. Temperature ( Cl Dissolved Oxygen (ppm) Results Temperature and oxygen -Temperature and oxygen profiles obtained in 1979 revealed two major thermal periods (Fig. 1). The entire water column at 4-l 2 C mixed during late fall, winter, and early spring (November- March). The summer stratified period (April-October) was characterized by epilimnetic temperatures of C. A slow erosion of the thermocline began in late August and continued until mixing was complete in November. Oxygen levels below saturation occurred in the lower waters during late winter (February-March), and a deoxygenated hypolimnion developed in April within 2-3 weeks of the onset of stratification. Oxygen maxima occurred at the epilimnetic-metalimnetic boundary, resulting in a positive heterograde oxygen curve in late summer. To look for possible long-term trends, we examined temperature profiles collected from 1978 to Over the 17-yr study period, a warming trend was detected at all depths and for the water-column average temperature (P2 = o. 10 C yr-l). The average rate of warming generally increased with depth and reflected a warming trend in winter air temperatures. Warming trends were generally weaker for upper water-column depths (l-3 m:,& = C yr-l; P = ) and stronger for lower depths (4-7 m: p2 = O.lO C yr-l; P = ) and the water-column average (& = C yr-l; P = ). The greatest rate of warming Fig Temperature and oxygen distributions with depth in was observed in hypolimnetic waters (0. 10 C increase per year at 7 m; Fig. 2). Mean annual hypolimnetic temperature was correlated with mean January air temperature (P = , R2 = 0.27). No positive trend was seen in annual mean air temperature for the Athens area (NCDC 1978-l 994), and there was no statistical relationship between mean annual water temperatures and summer air temperatures. The trend of increasing temperature did not occur at a consistent rate from year to year. An increase in water temperature and greater interannual variability seemed to occur in the mid-to-late 1980s. Figure 3 illustrates the relationship between the shallowest anoxic depth, defined as DO 5 1 mg liter-l, and time of year for all sampling dates with anoxia in (N = 222). When years for which we have early spring data (N = 8) are compared, hypolimnetic oxygen deficits consistently developed within a few weeks of stratification. Within 2-4 weeks oxygen was depleted from

4 Porter et al. B =: -2 E. Cu ocoo~o go0 amryo o oc&3 O 0 Ooo cm00 mzxt& 2-4 (D&pm 0 00zo 0 &oa, I.- -3 d COD 0 0 *Oa OCD 0ga 0000 an 00 0 o &I Year Fig. 2. Average annual temperatures (mean* SE) for watercolumn average temperature (O), mean 7-m temperature 0, and mean January air temperature (A) from 1978 to the stratified portion of the water column, resulting in an extensive anoxic zone below 2-3 m. These oxygen profiles illustrate that destratification begins in late August to early September, and that the water column does not become fully mixed until November. Rainfall- Seasonally, rainfall is distributed evenly throughout the year in the southeastern U.S. (Wallace et al. 1992). Average monthly rainfall data from 1979 to 1994 (NCDC 1978-l 994, data not shown) indicates that this general pattern holds true for the Athens area: monthly rainfall averages ranged from 8.4 to 11.9 cm. Monthly rainfall was highly variable among years (C.V. = 44-85%). Each month s rainfall deviated by more than 50% of its long-term mean in 5-10 of the 17 yr studied. Peak months showed no predictable pattern among years. In 1979, maximum rainfall occurred in April (20.6 cm; mean = 8.4 cm, median = 7.1 cm for all April ; NCDC ), and minimum rainfall occurred in December (3.5 cm; mean = 8.8 cm, median = 7.7 cm for all December ; NCDC ). Water chemistry-srp (Fig. 4) and TP (J. Meyer unpubl. data) concentrations fluctuated considerably (l-l 44 pg SRP-P liter-l and 16-1,080 pg TP liter-l) over the annual cycle. SRP concentrations remained low throughout the winter mixed period. Concentrations of SRP and TP were highest in midwater in April. These coincided with heavy spring rains, high sediment load, and high turbidity. During stratification, SRP levels decreased throughout the water column and remained low in the hypolimnion; TP increased with depth. Concentrations of ammonia N increased with depth after stratification and reached a maximum (1,400 pg N liter-l) at the end of stratification in October 1979 (Fig. 4). After complete mixing, ammonium concentrations declined at all depths, while combined nitrate and nitrite OCO 0 am.i.-li.--i.~l-- I I- I- l- FMAMJJASON Month ( ) Fig. 3. Extent of the anoxic zone on sample dates from 1978 through concentrations (J. Meyer unpubl. data) increased from - 1 pg N liter-l in September to 300 in February. In contrast to P, N concentrations did not increase during high rainfall in April After stratification, combined nitrate and nitrite concentrations declined to detection limits throughout the water column: first in the hypolimnion (May-June), then in the epilimnion (June-July), and finally in the metalimnion (July). Stratification led to a reduction of DIC in the epilimnion to a low of 0.95 mg C liter-l (Fig. 4), presumably due to the activity of photoautotrophs. Hypolimnetic release by heterotrophs increased DIC concentrations to a maximum of 32.8 mg C liter-l in October. The ph changed very little during the year (6.88kO.04) in spite of large changes in C02, indicating a high noncarbonate buffering capacity of the water. DOC (J. Meyer unpubl. data) remained relatively constant in surface waters (3.49k 1.3 mg C liter-l) despite major fluctuations in microbial biomass and productivity throughout the year (see below). Diurnal fluctuations in DOC were also minimal. In the hypolimnion, DOC concentrations were 4-6 mg C liter-l in May and increased to 19 by the end of stratification. Light, chlorophyll, phytoplankton, and photosynthesis - Light extinction coefficients remained relatively constant (1.O-3.8 m-l) throughout 1979, except during an influx of fine clay sediments following heavy rains in April (10.0 m-l; Fig. 5). Secchi disk depths, when determined across the past 16.5 yr, were generally between 0.5 and 1.5 with a maximum clarity of 3.5 m. Transparency was lowest during periods of heavy turbidity and red-brown color due to clay loading via surface water runoff. The frequency of clay-loading decreased in recent years, and water color was generally olive-green. Clarity was greatest in early winter after fall algal blooms. a3 D

5 Monomictic Lake Oglethorpe 1045 Soluble reactive liter -I) E lo-.- a g 8- $ 0 6- s.- 4- P.V I N M A y;tj 1400 ;FhlAM Ammonia (pg N liter - ) % E 1000 cn.- z 800 c z $ I I I lit-i NDJFMAMJJASONDJ Fig. 5. Annual variability in PAR light extinction coefficients and areal primary productivity rates in Dissolved Inorganic carbon (mg C liter -l ) Standing stock concentrations of HPLC chlorophyll a (Fig. 6)-a measure of photosynthetically active pigment-averaged 2 pg Chl a liter-l annually. Concentrations were higher in May through August, with a maximum of 29 pg Chl a liter-l in the upper metalimnion during June. Both algal and bacterial chlorophyll were found below the euphotic zone during summer stratification (Jacobsen unpubl. data; see also Parker 1995). Phytoplankton showed distinct seasonal and depth distribution patterns (Porter et al. unpubl data). Early in the winter mixed period, phytoplankton were distributed relatively evenly throughout the water column and the assemblage was composed of small and colonial flagellates (chrysophytes and cryptomonads), diatoms, green algae, and large flagellates (dinoflagellates and euglenoids). In the early part of the stratified period, chrysophytes, cryp- Fig. 4. Depth distributions of soluble reactive P, ammonia, and dissolved inorganic C concentrations in 1979.

6 1046 Porter et al. Chlorophyll a (pg liter-l) V,, (nmoles liter -1 h -l) Particulate ATP (pg liter -l) tomonads, and green algae dominated the algal assemblage, but filamentous cyanophytes and large (>20-pm GALD) algal flagellates (dinoflagellates and euglenoids) were the major components of the phytoplankton for most of summer. Large motile flagellates were found in the euphotic zone during stratification and cyanobacteria generally settled to the epilimnetic-metalimnetic boundary. These general patterns were also found in more recent studies of phytoplankton succession in Lake Oglethorpe (Parker 1995). Integrated photosynthesis expressed on an areal basis (Fig. 5) was highest from May to September (470 mg C m-2 d-l in June and 1,420 in August). The first peak in primary productivity occurred in May (900 mg C m-2 d- l), as stratification stabilized and while phytoplankton biomass was still moderate. A second peak was observed in August (1,420 mg C m-2 d- ) as the epilimnion deepened and algal cells and nutrients that had accumulated in the metalimnion were dispersed into the cuphotic zone. Winter primary productivity remained moderate during October-February (loo-470 mg C m-2 d-l). Productivity rates were lowest in March and April (40-70 mg C m-2 d-l). Primary productivity rates did not correlate with HPLC chlorophyll a or cell concentrations (areal chlorophyll data not shown, but see Fig. 6). On most dates, maximum photosynthetic rates were at the surface, while maximum algal cell and active Chl a concentrations were at 2-3 m (Fig. 6). Annual primary production for 1979 was -500 g C m-2 yr-l. Microbial abundance and production -Indicators of microbial biomass and activity showed distinct seasonality and patterns of vertical distribution during the stratified period. Concentrations of bacteria in the water column ranged between 1.5 x lo6 and 3.2 ~ lo7 cells ml-l, with an average of 94% small unattached coccoid cells (Porter and Feig 1980). Densities were lowest in winter and highest during summer stratification in the hypolimnion (Fig. 6). Throughout the year, bacterial densities were lowest at the surface. During late fall and winter, bacteria were uniformly distributed with depth. During the stratified period, concentrations of bacteria were highest immediately below (June-July) or just above (August- September) the interface between the epilimnion and the metalimnion. Heterotrophic potential, the maximal uptake and mineralization of [ 14C] glucose ( V,,,), was measured throughout 1979 as a relative indicator of bacterial production rates (Wright and Hobbie 1966). Values of V,,, were low and uniform throughout the water column during late fall and winter In April V,,, increased dramatically at all depths, peaking at 1 m. This coincided with peak SRP values and low light availability in that year (Fig. 4). During the stratified period, values were high in the lower D J F M A M J ii S 0 N D Fig. 6. Seasonal and depth variation in HPLC chlorophyll a, heterotrophic potential (V,,,), bacterial cell numbers, and particulate ATP in 1979.

7 stable bounda nion was at 3 F hrlamjja r-.r- SONDJFMA 1 were as e lationship between rainfall and sedimentation in the tentral deep-water basin. ber-march) and stratified (Apri consistently from ye presence of an extensive anoxic hypolimnetie zone are autotrophic and het- The average annual has any measurable impact on biological variables in the 979, clay loading diminished predictable in the following

8 1048 Porter et al. winter mixed period. In particular, measurements of both nutrient concentrations and primary production rates suggest high activity in winter compared to colder lakes. SRP is low throughout winter, indicating that available P is rapidly incorporated into the biotic pool. Increases in nitrate and nitrite concentrations throughout the water column in winter, and corresponding decreases in ammonium concentrations, indicate that nitrifying bacteria are active during the mixed period. From October to February, areal primary productivity rates (loo-470 mg C rnb2 d-l, see Fig. 5) are about equal to those in hypereutrophic Wintergreen Lake (Wetzel 1983). However, during this same time period Chl a concentrations are similar to those in oligotrophic Lawrence Lake (Fig. 6; Wetzel 1983). Production per unit algal biomass is therefore high, and this is presumably a result of relatively high water temperatures, light availability, physical mixing, and also rapid turnover due to grazing (see below). Algal productivity throughout winter may retain nutrients in the biotic pool and reduce the potential magnitude of spring algal blooms. Compared with those in northern lakes (Wetzel 1983, table 15.9), daily rates of primary productivity in Lake Oglethorpe (100-l,420 mg C m-2 d-l) were in the mesotrophic range, while annual productivity (500 g C m-2 yr-l) was in the eutrophic range. This was due to the extended growing season. Summer heterotrophic production -Heterotrophic activity is important throughout the summer stratified period. Deoxygenation of the hypolimnion is rapid (2-4 weeks) after the onset of stratification. Seasonal patterns of heterotrophic production measured by glucose uptake in 1979 (V,,,, Fig. 6) were confirmed in with tritiated thymidine and leucine tracers (McDonough et al. 1986). Highest rates were correlated with high Chl a concentrations at the epilimneticmetalimnetic boundary, which was not a region of high bacterial or protozoan abundance (Fig. 6; Pace 1982) but was a region of high protozoan and metazoan grazing activity (Sanders et al. 1989; Bennett et al. 1990). Hence, bacterial production and standing stock were not correlated. Bacterial production may be directly supported by high concentrations of filamentous algae at the interface between the aerobic epilimnion and the anaerobic hypolimnion. DOC concentrations remained moderate and relatively constant throughout the year in the mixed portion of the water column ( mg C liter- ) but increased in the hypolimnion after stratification. Organic sedimentation was highest at the epilimnetic-metalimnetic boundary in midsummer. Decreasing organic sedimentation with depth, and also declining ATP concentrations in the metalimnion and hypolimnion in summer, suggest decomposition of organic matter within the water column, rather than in the sediments. In the anoxic zone, bacteria may also receive carbon via grazing activity. Heterotrophic microflagellates are abundant in the hypolimnion during stratification and peaked at summer densities of 102-lo4 cells ml-l in the metalimnion (Bennett et al. 1990). Distinct assemblages of protozoa are also found in the anoxic hypolimnion (Pace and Orcutt 1981; Pace 1982). In addition, hypolimnetic SRP concentrations declined throughout summer stratification while TP increased, which is different from observed SRP accumulations in north-temperate lakes with anoxic hypolimnion (Wetzel 1983; Caraco et al. 1991; Krambeck et al. 1994). Preliminary in situ EPA dome studies in Lake Oglethorpe (R. Raschke unpubl. data) indicate P release by anoxic sediments during summer stratification. It is possible that P does not accumulate because it is retained in the active heterotrophic biota of the hypolimnion. As an indicator of high biological activity, this trend suggests that the observed hypolimnetic increase in DOC represents an accumulation of refractory compounds. Seasonal shi$ in the dominance of macro- vs. microzooplankton -The pelagic community is dominated by crustacean macrozooplankton in winter and protozoan and metazoan microzooplankton in summer (Pace and Orcutt 1981). These seasonal differences in zooplankton community structure reflect differences in the dominant size and quality of food available during mixis and stratification (Fig. 8). The algal groups characteristic of winter months were primarily small, high food-quality species. The discrepancy between moderate productivity rates and low algal biomass accumulation can be explained by the grazing of crustacean zooplankton, especially cladoceran species, which accumulated biomass in winter (4-60 animals liter-l in 1979; Orcutt and Pace 1984). At this time, bacterial numbers are low, and bacteria and bacterial consumers are minor supplements to algal resources for crustaceans (Pace et al. 1983). Cladocerans were inefficient as direct consumers of bacteria, contributing < 1% to community grazing (Sanders et al. 1989). Mixotrophic flagellates are the major bacterial grazers during winter mixis (Bennett et al. 1990). After the major biomass peaks in fall and winter, cladoceran population densities exhibit a smaller density pulse in late spring (April) and are at low densities by early summer (Pace and Orcutt 1981; P. Saunders unpubl. data). This is contrary to the pattern observed in northern dimictic lakes, where the spring-summer bloom usually has the greatest abundances (Horne and Goldman 1994). In June 1979, there was an abrupt decline in crustaceans, particularly Daphnia, and crustacean populations remained low until October. The early summer decline in crustaceans cannot be attributed to high temperatures (Orcutt and Porter 1983, 1984). Shifts in food quality, with a reduction of small edible algae and an increase in bacteria not suitable for growth and reproduction of Daphnia are in part responsible for the declines (Pace et al. 1983). Increases in blue-green algal filaments that are energetically costly for cladocerans to reject (Porter and McDonough 1984) also occurred in late spring. A model by Pace et al. (1984) predicted that Chaoborus can also have a significant impact on Daphnia numbers and life histories in the early (April-May) part of the stratified period. Whatever the cause of low crustacean numbers, one consequence is that the clear-water phase that occurs in early summer in many northern dimictic lakes due to grazing by crustacean zooplankton populations

9 Monomictic Lake Oglethorpe 1049 (Luecke 1990) has not been observed on Lake Oglethorpe. This cannot be explained by the presence of clays, since a clear-water phase has not been observed in recent years that lack significant clay loading (Parker 1995). Dominance of the zooplankton biomass by rotifers (2-80 x 1 O2 animals liter- l, Orcutt and Pace 1984) and protozoans (104-1 O5 cells liter- l; Pace and Orcutt 1981; Pace 1982) during summer stratification was correlated with increases in bacteria as a resource base (Pace and Orcutt 1981). Flagellated protists, the major bacterivores in the lake (Sanders et al. 1989), were not significantly correlated with bacterial densities (Bennett et al. 1990). The presence of high densities of rotifers, which were found to contribute 68-92% of community grazing on heterotrophic flagellates (Sanders et al. 1994), may have led to the low correlation between bacteria and flagellates. Rotifers also fed on some algae, ciliates, and bacteria. Rotifers are therefore likely major links between bacterial production and higher trophic levels during summer stratification. High abundances of rotifers and protozoans seem to also occur in tropical and subtropical lakes (Serruya and Pollingher 1983; Bays and Crisman 1983) and may be a consequence of enhanced microbial production. Rotifers are fed upon by Chaoborus and larval fish (Porter 1996; Bruce unpubl. data; Saunders unpubl. data). It may be that the early planktivorous life stages of larval bluegill, which are produced throughout summer in Lake Oglethorpe, are supported significantly by microbially based production. Thus, microbial production may ultimately be supporting a bass-bluegill fish assemblage similar to that of many northern lakes. Rotifers can interact with Daphnia populations directly through competition (Gilbert 1988) and indirectly by providing food for high numbers of predatory Chaoborus (Neil1 1985; Porter 1996). In summer, therefore, microbially based production may have a bottom-up effect as a resource base, a lateral effect (Porter 1996) via interconsumer competition, and a top-down effect by supporting predators such as Chaoborus and larval fish. Extensive anoxia and the habitats of higher trophic consumers-the rapid development of anoxia below 2-3 m following thermal stratification may be significant to the survival of pelagic fish, the invertebrate predator Chaoborus, and crustacean zooplankton. Extensive hypolimnetic anoxia is probably an important habitat limitation for both crustacean zooplankton and centrachid fish of Lake Oglethorpe. Early anoxia in the lake may also provide Chaoborus with an important refuge from fish predation. This refuge and ample microbially based resources may allow Chaoborus to reach the exceptionally high abundances, up to 10 liter-r and 20,000 m-2, found in the lake throughout summer (Porter 1996). Predictions for dimictic lakes-if climatic warming continues, the seasonal patterns observed in Lake Oglethorpe could be used as predictors of possible ecological changes in north-temperate lakes. The loss or reduction of winter ice cover would increase light availability, and longer periods of winter mixis would reduce sinking losses for 7 HETEROTROffllC f I I FUGELLATES MIXOTROPHIC FIAGELIATES FALL- WINTER-SPRING SUMMER Fig. 8. Food-web relationships during the fall-winter-spring mixed period and the summer stratified period in mesoeutrophic, monomictic Lake Oglethorpe (after Porter 1996). During mixis, high-quality algal food supports abundant populations ofcrustaceans, particularly the cladoceran Daphnia spp. In summer, microbially based production (protozoans, rotifers, small cyclopoid copepods, and Chaoborus punctipennis larvae) supports planktivorous fish and their larvae. phytoplankton. These and warmer winter temperatures may enhance nutrient cycling and primary productivity rates. Crustacean zooplankton populations would grow during the ice-free period. Nutrients would accumulate in the biota, rather than in the lower waters as in icecovered systems, because of physical mixing, increased winter productivity, and biomass. Therefore, nutrients may be less available to support a spring algal bloom. Bacterial production would increase and its consumers (flagellates, ciliates, and rotifers) would dominate zooplankton biomass in summer. Heterotrophic production would be particularly important to zooplankton in summer if autotrophic production were primarily by large, inedible forms, such as blue-green filaments, dinoflagellates, and euglenoids. Anoxia in the hypo- and metalimnion would develop earlier in the stratified period, which may restrict the habitats of both crustacean zooplankton and fish, while providing a refuge for the anoxia-tolerant predator Chaoborus. If stratification, anoxia, and the shift to a microzooplank-

10 1050 Porter et al. ton-dominated zooplankton community occurs before water temperatures allow significant fish activity, crustacean zooplankton may decline before fish populations can utilize them for growth of early life stages. On the other hand, microzooplankton and Chaoborus may provide an alternative resource base for larval and adult fish, such as the bass-bluegill assemblage in Lake Oglethorpe and many northern lakes. Potential responses of northern, dimictic lakes to climatic warming would not require new associations or processes by this analog model. In general, conditions that prevail in northern lakes at the end of summer (August) would be expected to extend throughout more of summer in the event of continued climatic warming. Overall, we predict that climatic warming would tend to shift patterns in northern dimictic lakes toward those observed in southern monomictic lakes. This pattern should be enhanced with increasing eutrophy. 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