Nitrogen Fixation in an Oligotrophic, Saline Desert Lake: Pyramid Lake, Nevada

Nitrogen Fixation in an Oligotrophic, Saline Desert Lake: Pyramid Lake, NevadaAuthor(s): A. J. Horne and D. L. GalatSource: Limnology and Oceanography, Vol. 30, No. 6 (Nov., 1985), pp. 1229-1239Published by: American Society of Limnology and OceanographyStable URL: http://www.jstor.org/stable/2836477 .

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Limnol. Oceanogr., 30(6), 1985, 1229-1239 ? 1985, by the American Society of Limnology and Oceanography, Inc.

Nitrogen fixation in an oligotrophic, saline desert lake: Pyramid Lake, Nevada

A. J. Horne Aquatic Ecology Group, Division of Sanitary and Environmental Engineering, University of California, Berkeley 94720

D. L. Galat Department of Zoology, Arizona State University, Tempe 85287

Abstract

High rates of nitrogen fixation by a short-lived but dense unialgal bloom of the planktonic blue- green Nodularia spumigena provided 99.5% of the alga's needs and 81% of Pyramid Lake's annual total combined nitrogen input in 1979. The bloom was spatially very heterogeneous. Bloom size, duration, and presumably N2 fixation vary from year to year, but in 1979 about 900 t of nitrogen were fixed in 2 months in this large deep lake. The annual rate of N2 fixation was about 2 g m-2. In this year of low inflow the Truckee River provided 54 t of inorganic nitrogen and 83 t of organic nitrogen. Planktonic N2 fixation has not been measured during high inflow years and may have been small relative to river input. Lakewide average heterocyst to vegetative cell (h: c) ratios followed seasonal trends in N2 fixation, but synoptic samples showed only a weak relation between h: c and N2 fixation. N2 fixation was induced by low epilimnetic levels of inorganic nitrogen and ended before lake overturn in the fall. High rates of N2 fixation were confined to the upper 5% of the epilimnetic volume and thus occurred only in calm weather when Nodularia colonies floated to the lake surface. Access to freshly dissolved atmospheric CO2 may account for the near-surface dependence, since the lake pH is normally about 9.2. We predict that Nodularia will not show the same degree of near-surface dependence in near-neutral lakes or in the ocean.

It would be useful to forecast accurately the occurrence and magnitude of aquatic N2 fixation. Nitrogen fixation by blue-green algae is common but its occurrence often bears no obvious relationship to the fertility of the system. For example, N2 fixation by planktonic or attached algae has been measured in very oligotrophic tropical ocean waters (Carpenter and McCarthy 1975) and oligotrophic lakes (Loeb and Reuter 1981) as well as in mesotrophic estuaries (Ostrom 1976), mesotrophic lakes (Home and Fogg 1970; Granhall and Lundgren 1971), and highly eutrophic lakes (Home and Goldman 1972). It occurs in tropical (Home and Vi- ner 1971), Mediterranean (Home et al. 1979), temperate (Torrey and Lee 1976; Home 1978), Antarctic (Home 1972), and Arctic waters (Alexander and Schell 1973).

Although nitrogenase synthesis is facili- tated by a low ratio of cellular nitrogen to carbon, there is no indirect method to de- termine this ratio. Since levels of nitrate or ammonium in the environment do not give a reliable guide to the need for N2 fixation,

there is no simple method to predict that the process will occur in any given system.

Where N2 fixation does occur, its quantitative importance may be more predict- able. For example, lakes in semiarid climates often have lower N: P ratios than those in wet climates (Goldman and Home 1983). Thus, lakes in arid zones, regardless of their trophic state, may depend more on N2 fixation than lakes in wet climates.

We examined this concept in Pyramid Lake, Nevada, a desert lake with no outflow (Fig. 1). Several recent studies of the lake and its tributaries provided much of the information needed to construct the required nutrient budgets (for details, see Hamilton- Galat and Galat 1983). Pyramid Lake is large and is the deepest saline lake in the western hemisphere (A = 446 kM2, Zmax = 103 m, Z = 59 m). It is considered oligotrophic. In the late 1970s, its photic zone averaged 11 m, chlorophyll a 3.3 ,ug liter-', and net phytoplankton photosynthesis was 506 mg C m-2 d-l (Galat et al. 1981). It is nitrogen depleted and phosphate-rich, with a mean

1229



1230 Horne and Galat

x~~~~~~ /

IO\ ~~~L60 x f 10

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\ x HOLNEY

9

RENO x to TRUCKEE

7

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4 PYRAMID

xW~L. TAHOE

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Fig. 1. Sketch map of the Pyramid Lake region and depth contours of the lake in meters. Several nearby saline lakes are shown which contain Nodularia.

epilimnetic average for total combined inorganic nitrogen <40 ,ug N liter-' and soluble reactive phosphate > 80,ug P liter-1. In 1979, the Truckee River supplied 1.6% of the total lake volume.

Pyramid Lake is a graben lake, deeper than most lakes where high rates of N2 fixation have been measured. Its relatively high altitude (1,157 m) and large volume result in a maximum epilimnetic temperature of only 24?C, despite summer air temperatures >3 5?C. The lake stratified thermally between June and mid-October 1979, with a thermocline at about 20 m. Complete overturn occurred by year's end. In some years, including 1979, there are large conspicuous blooms of the colonial, planktonic blue- green alga, Nodularia spumigena. The presence of Nodularia in Pyramid Lake and adjacent waters is largely due to the alga's tolerance of moderate salinity. Pyramid Lake's volume has been substantially re- duced since 1905 due to diversion of about half of its inflow for agriculture. Salinity rose from 3.8%oo in 1933 to 5.3 in 1979. Inflow during 1979 was the second lowest of the decade. In summer 1977 and 1979, the bloom of Nodularia persisted for a few months. There was no bloom in 1980, a year of average inflow, but there was a bloom in 1983 following the largest inflow of this cen- tury.

Nodularia spumigena is characteristic of moderately saline waters (Nordin and Stein 1980) and is common in deep and shallow saline lakes as well as in brackish seas (Hutchinson 1967; Horstmann et al. 1978). Nodularia forms surface accumulations as do other bloom-formers (Reynolds and Walsby 1975) and fixes nitrogen (Fogg et al. 1973).

We thank M. L. Commins for the Nod- ularia counts and M. Coleman and K. Ham- ilton-Galat. Partial funding for this project was provided by the U.S. Bureau of Indian Affairs, a University of California 615 grant, and the Sanitary Engineering and Environ- mental Health Research Laboratory. D. L. Galat carried out fieldwork while at the Col- orado Cooperative Fishery Research Unit, Colorado State University. We appreciated reviews by P. L. Brezonik, W. M. Lewis, Jr., and H. W. Paerl.

Methods N2 fixation in the plankton was estimated

with an acetylene reduction technique in situ (Stewart et al. 1967; Home and Goldman 1972). For convenience, we use the terms N2 fixation or nitrogenase activity even though we measured only the reduction of acetylene to ethylene by nitrogenase. We used the ratio of three molecules of ethylene



N2 fixation in Pyramid Lake 1231

released per one molecule of gaseous nitrogen fixed by the enzyme (Hardy et al. 1968).

Water from the pelagic zone was collected every month from May until August and every few days from early September to late October. Nodularia was rare before 11 Sep- tember and some samples were concentrated 10-fold to 20-fold with a 25-,um-mesh screen. For the quantitative study made after 9 September, we used unmodified samples because net concentration can give er- roneous results (Leonardson 1983). Monthly collections were made with a syringe sampler which integrates water from the entire photic zone, as determined from measurements of algal photosynthesis in situ. Water was collected from three well spaced stations in the lake and the three samples were incubated at 4.5 m. The sites were at central locations along the long axis of the lake. Additional samples collected at the same three stations at depths of 0, 1.5, 4.5, 7.5, 1 1, and 15 m beginning on 9 September were incubated separately in situ at the depths of collection.

Because most of the Nodularia was often concentrated in the few centimeters below the lake surface, we measured N2 fixation in surface samples as well as throughout the water column. At the height of the bloom on 25 September, we collected 25 widely spaced samples. The boat was slowed down so that bow waves did not disturb the surface layer of Nodularia; standing near the bow, we dipped a 20-liter bucket at random into the slowly passing water. The upper 10 cm of lake water were collected and sub- sampled for measurements of nitrogenase activity and algal abundance. The bucket- dip method overcomes small-scale (-cm) patchiness better than a tube sampler. For a large lake, the technique gives a more ac- curate, if less precise, estimate of the total N2-fixing potential than any other method.

Water samples of 1 00-cc volume were en- closed in 123-cc glass bottles sealed with serum stoppers. Acetylene was generated on site from calcium carbide and 10 cc of gas injected into each bottle via the serum stopper. The bottles were gently shaken to equil- ibrate the acetylene with the lake water. The gas space above the sample buffers CO2 and 02 changes in the water which otherwise

occur rapidly in sealed bottles. Plankton samples were normally incubated in situ for 2 h starting near noon in light bottles only; gas samples were then withdrawn into 0.5- cc glass syringes with plastic plungers, sealed temporarily by inserting the needle into a rubber stopper, and analyzed within a few hours, using a Varian 1200 gas-liquid chro- matograph calibrated each day with a standard gas mixture (1.5 ppm of ethylene, balance argon). We used a dilution series with air and pure ethylene to check the accuracy of the standard gas mixture. The level of detection for Pyramid Lake samples was between 1 and 10 nmol C2H4 liter-' h-1. We estimated baseline ethylene levels due to natural background and trace contamina- tion from acetylene generation on all oc- casions from triplicate lake samples killed with mercuric chloride before acetylene ad- dition and incubation.

In 1979 lake nitrogen (nitrate, nitrite, ammonium, total Kjeldahl) and phosphorus (reactive and total) levels were monitored as part of a larger project (Hamilton-Galat and Galat 1983). Fluvial nitrogen inputs to the lake were estimated from continuous discharge gauging and from monthly chem- ical analysis of grab samples of the major inflow to the lake, the Truckee River (U.S. Geol. Surv., Univ. Nevada, Desert Re- search Inst. unpubl. data). Because the flows of the Truckee River are closely regulated to prevent flooding and there are dams on all significant tributaries and on Lake Ta- hoe, the discharge is less variable and the monthly samples are more representative than for most rivers. Records of the various nitrogen fractions (total organic, nitrate, nitrite, and ammonium) have been collected over the length of the Truckee River for more than a decade. The 1979 data are con- sistent with the multiyear relationship of discharge to nutrients. We consider the records adequate for annual budget purposes. River inflow dominates all other nitrogen sources except for N2 fixation. Minor nitrogen inputs were measured as described below.

Surface runoff and groundwater nitrogen inputs were calculated from the average annual discharge to the lake (12.3 x 106 m3:

Van Denburgh et al. 1973) and the average




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Fig. 2. Lower panel: seasonal variation of N2 fiX- ation (+, shaded, measured as nitrogenase activity) and heterocyst-to-vegetative-cell ratio (0). Upper panel: biomass (+, settled volume) and cell numbers (0) for Nodularia spumigena in Pyramid Lake in 1979. The time of the 25-station synoptic study (Fig. 5) is shown by an open arrow and those of satellite photographs by solid arrows.

nitrate content of groundwater (0.31 mg N liter-', from 1982 records of Pyramid Lake Paiute Indian Tribe). We measured the total nitrogen content of precipitation at Pyramid Lake in 1979 (mean, 0.47 mg N liter-1) and multiplied this by the total precipitation falling on the lake for that year (11.6 x 106

mi3). Nitrogen influx from dry fallout and tumbleweed was calculated by multiplying their measured C: N ratios (9.7 and 44.0) by the 1977 estimated total carbon inputs of 14 t for dryfall and 2,135 t for tumble-

weed (Galat et al. 1981). A maximum influx of domestic waste from Sutcliffe, Ne- vada, was determined from the town's 1979 population of 333 and the average per capita total nitrogen content of human sewage (4 kg yr-': Fair et al. 1968). The nitrogen content of feces from white pelicans and dou- ble-crested cormorants, which nest on An- aho Island, was estimated from the literature (Hutchinson 1950). The bird population es- timates for Anaho Island were obtained from Anderson (1982). An annual nitrogen influx was approximated from this value from as- sumptions concerning bird residence times at Pyramid Lake and the proportion of their food that was eaten at locations other than Pyramid Lake. Nitrogen gains from Lahon- tan cutthroat trout were calculated from 1979 stockings (Pyramid Lake Indian Trib- al Enterprises unpubl. data). The nitrogen content of trout biomass was estimated to be 2.5% per unit wet weight (Niimi 1972).

Heterocysts and vegetative cells were counted microscopically. During the bloom, the volume of Nodularia could be measured directly as settled volume in a graduated cylinder (100-500 cc). Satellite pictures showing the near-infrared 715-nm reflec- tance band characteristic of blue-green phytoplankton (Anderson and Home 1975) were obtained from LANDSAT.

Results Planktonic N2 fixation was negligible un-

less Nodularia was present (Fig. 2). Soon after appreciable numbers of Nodularia fil-

NITROGEN FIXED ( n mol C2H4 liter-I h-)

0 500 200 0 200 400 0 100 200 0 200 500 0 100 o - l 0z- 1tt I 1 4 7 7 26 10 26

E 5 5 ^E 5jSEP XSEP SEP SEP OCT |OCTk

0 1 10 w

15 15

Fig. 3. Vertical distribution of N2 fixation over the course of the bloom. Error bars are ?2 SD and, where not shown, are smaller than the width of the dot.




aments were observed in late August, N2 fixation rates rose; high rates were confined to the brief period of dense Nodularia pop- ulations. Fixation ceased in late October, well before lake overturn.

At the low Nodularia densities before the bloom, rates of planktonic N2 fixation per unit lake surface were a few tenths of a mmole of C2H4 m-2 d-l. During the bloom period, values rose to between 3 and 5 mmol C2H4 m-2 d-l (Fig. 2). At this time, short term rates per unit volume ranged from 4 to 400 nmol C2H4 liter-' h-' (Fig. 3), and in very dense patches (Fig. 4) surface rates exceeded 50 x 103 nmol C2H4 liter-' h-I (Fig. 5). N2 fixation augmented total organic nitrogen levels in the lake by almost 0.5% per day during the bloom period. The annual influx of nitrogen to the lake per unit area from N2 fixation was calculated to be 20 kg ha-' (2 g M2 yr'1).

Initially, Nodularia filaments had few heterocysts, but during the bloom, ratios of heterocysts to vegetative cells (h: c) were high, between 1: 12 and 1: 50. The change in h: c ratio closely followed changes in rates of N2 fixation for the photic zone (Fig. 2). The highest N2 fixation rates occurred with the highest h: c ratios, and lower, but still high, rates were found at the lowest h: c ratios. This planktonic Nodularia bloom shows h : c variation in relation to N2 fixation similar to that of another planktonic cyanophyte (Aphanizomenon flos-aquae), but contrasts with the pattern for Anabaena (fig. 3 in Horne and Goldman 1972).

Nitrogen fixation was usually confined to the upper 5% of the photic zone-a layer <50 cm thick. However, in the early stages of the bloom, levels of fixation were relatively low down to 6 m (Fig. 3). On windy days, Nodularia was present as single filaments or relatively small bundles of filaments. On calm days during the bloom, surface accumulations of Nodularia were extremely dense due to the bunching of loosely adhering filaments coupled with buoyancy provided by gas vacuoles (Fig. 4). The algae frequently dominated the ap- pearance of the lake (Fig. 4), but Nodularia filaments were not observed in the epi-neus- ton.

Inorganic nitrogen concentrations were

z z.

V.~~~~~~~~~~~~~~~~~~.j

Fig. 4. Surface Nodularia accumulations at mid- morning 23 September 1979 during synoptic study. Above: mesoscale (X 1 m) and microscale (X 1 cm) patchiness. Below: effects of a small stone dropped onto a surface accumulation. The strongly adhering Nodularia stands are apparent. The layer was about 1 cm thick.

low throug-hout the period when Nodularia was present and were very low during the period of intense N2 fixation (Table 1). However, N2 fixation ended well before the annual increase in surface nitrate, which occurs as the thermocline begins to descend in November. In contrast, soluble reactive phosphate was relatively abundant and re- mained constant at about 70 gtg liter-' P04-P. The dissolved inorganic nutrient ratio of N:Pwas about 1: 2.




HE TEROCYSTS

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Fig. 5. Horizontal synoptic distribution of nitrogen fixation, heterocysts, settled volume, and vegetative cells of Nodularia on 23 September 1979. Radius of circle indicates amount. Photograph shows near-infrared reflec- tance of surface Nodularia on 26 September.

Rates of nitrogenase activity in 25 surface samples collected synoptically on 23 Sep- tember 1979 varied by four orders of magnitude, from 5 to 53,000 nmol C2H4 liter-' h-I (Fig. 5). Surface N2 fixation averaged for the whole lake was 7,200 nmol C2H4 liter-' h-1. High rates of N2 fixation and algal patches were widely distributed throughout the lake, but there was no obvious relation

between N2 fixation and biomass (Fig. 5). Short term rates of N2 fixation were not related to the ratio of heterocyst to vegetative cell (r2 = 0.006). Possible reasons for this are given in the discussion. However, there was some relationship between the numbers of heterocysts present and N2 fixation (r2 = 0.39, Fig. 5). This correlation is much weaker than normally found among




Table 1. Average concentration of major nutrients in the epilimnion of Pyramid Lake in 1979 (values in ,ug liter-'). Phosphate was measured as soluble reactive phosphorus.

May Jun Jul Aug Sep Oct Nov

N03-N 20 20 30 10 10 10 70 N02-N <5 <10 <10 <10 <5 <5 <5 NH4-N 15 10 <10 <20 20 <20 <20 P04-P 70 70 70 70 80 60 70

other heterocystous genera (Torrey and Lee 1976; Home et al. 1979; Levine and Lewis 1984).

Both direct field and remote-sensing measurements of the surface Nodularia bloom show considerable spatial heterogeneity (Fig. 5). From the boat we observed areas of several square kilometers covered with a yel- low-green Nodularia layer about 3-5 cm thick; 910 cc of settled algae per liter was recorded for one sample. Bloom distribution as indicated by remote sensing shows algal layers as white, which in the photograph in Fig. 5 probably corresponds to a surface layer with more than 0.5 cc of settled

2000

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Z 10 0 %% A /

5 V

z ~~~~~~_J

0

Z 1 ci 0.5 0 cc 0.2 z

J F M AMJ J A SON D MONTH 1979

Fig. 6. Relatioxiship between monthly nitrogen loadings from the Truckee River and N2 fixation in Pyramid Lake. All other sources of nitrogen input are negligible (Table 2). Total N is shown as a broken line; shaded area indicates inorganic N (NH4+ + N03- + NO2j); N2 fixation is shown solid.

Nodularia volume per liter. Microscopic ex- amination of 400 samples collected during the bloom period showed an almost unialgal stand of Nodularia; zooplankton was found only in subsurface samples where Nodularia was rare.

We calculate that in 1979, 99.5% of the nitrogen used in producing the large Nod- ularia bloom was derived directly from the air. During the 2 months of the Nodularia bloom, 866 t of nitrogen were fixed while only 4.4 t of inorganic nitrogen, mostly nitrate, arrived via the Truckee River (Fig. 6). Recycling within the epilimnion is not a likely source of N for the growth ofthe bloom since there was almost no phytoplankton to recycle in this oligotrophic lake before the Nodularia bloom. Fixation accounted for 81% of the whole lake's nitrogen budget in 1979 (Table 2). Measurement of a nitrogen budget for Pyramid Lake is easier than for most lakes due to the few inflows and to the desert environment which drastically re- duces nitrogen from surface and groundwater seepage as well as from riparian vege- tation. Sediment N2 fixation is probably negligible (Galat and Home unpubl.).

Table 2. Calculated annual nitrogen balance for Pyramid Lake in 1979. Units are tonnes of N per year. We assume that some nitrogen in fish removed by >10,000 birds inhabiting the area is returned to the lake.

Gains

N2 fixation 866 River inflow 75 Surface flow + groundwater 3.8 Rainfall on lake 5.4 Dry fallout 1.4 Domestic waste 1.3 Tumbleweed 49 Bird droppings 3.4 Fish stocking 1.1

Total 1,006.4




Discussion

Nitrogen fixation is important to the annual nitrogen budget of the arid-zone Pyr- amid Lake. The role of nitrogen as a limiting factor for terrestrial organisms is well known (Cole 1968; Home 1972), but Pyramid Lake seems to be unusual in that almost all of its nitrogen was derived from N2 fixation in the year of our study. However, the per- centage of annual nitrogen input due to N2 fixation is similar to the 82% found for two Swedish lakes (Granhall and Lundgren 1971, recalculated; Leonardson and Bengtsson 1978) and the 30-70% value found for Clear Lake, California, in the decade after 1969 (Home and Goldman 1972; Home unpubl.).

River discharge was low in 1979 so the results reported here may be atypical. Total nitrogen inflow from the Truckee River was 75 t in 1979 and over 640 t in 1980. There was no large Nodularia bloom in 1980 and, we assume, no N2 fixation. In 1983, a year of record high inflow (and presumably high nitrate) to Pyramid Lake, there was a large Nodularia bloom. Thus, the relationship between Nodularia blooms, N2 fixation, and river nitrogen inflow is not straightforward in Pyramid Lake.

The large contribution of N2 fixation to the lake budget was due to the lack of other nitrogen inputs, not to an unusually high rate of N2 fixation. The higher daily rates recorded for Pyramid Lake in 1979 were 3- 5 mmol C2H4 m-2 d-l during the bloom period, similar to values of 1-14 mmol C2H4 m-2 d-l found for shallow, warm eutrophic lakes (Home and Viner 1971; Ganf and Home 1975). Some values for the Baltic Sea are much lower: 6-80,umol m-2 d-l (Rinne et al. 1981). Many workers on stratified lakes and the ocean express N2 fixation only as ethylene produced per hour near noon. In several lakes and the Baltic Sea when Nod- ularia is present, N2 fixation ranges from 0.6 to 300 nmol C2H4 liter-' h-l (Rusness and Burris 1970; Liinnergren et al. 1974; Torrey and Lee 1976; Lindahl et al. 1980; Rinne et al. 1981), although much higher values are recorded occasionally (Htibel and Htibel 1980). In comparison, values at Pyr- amid Lake were almost three orders of mag-

nitude higher (7-53 Amol C2H4 liter-l h-1), but overlap with peak values from the Baltic Sea. A typical maximum rate of N2 fixation of about 0.5% increase in total N per day is commonly reached in blooms of blue-green algae (Home and Fogg 1970). This rate was reached during bloom peaks in Pyramid Lake in 1979.

High nitrogenase activity in the plankton of Pyramid Lake occurred only during the most stratified conditions when the population was packed into a layer just below the lake surface, an unusual distribution although it often occurs in other lakes at in- tervals during a bloom (Reynolds 1971). We postulate that once conditions suitable for N2 fixation are present (low inorganic nitrogen, adequate phosphate, and soluble iron), N2 fixation depends on calm periods when Nodularia floats to the surface. An obvious advantage of growth near the surface is access to freshly dissolved atmospheric C02, discussed elsewhere (e.g. Wals- by and Booker 1976). Free CO2 may be in short supply in Pyramid Lake despite a DIC of 1,160 mg liter-l (HC03- + C032-) main- ly because of the constant and high pH (annual average = 9.2: Peng and Broecker 1980). The lake is well buffered and the largest pH changes recorded were between 9.0 and 9.4 during Nodularia blooms. The lake also loses free CO2 by CaCO3 precipitation during lake whiting events (Berg et al. 1981). Paerl and Ustach (1982) have shown that some blue-green algae prefer CO2 over HC03- and thus would benefit greatly from a near-surface bloom in Pyramid Lake.

The near-surface dependence of Nodu- laria in Pyramid Lake distinguishes it from most N2-fixing genera, Aphanizomenon, Anabaena, Oscillatoria (Trichodesmium), and Gloeotrichia. Near-surface light conditions usually damage planktonic algae un- less they have some protection. The protection mechanism, if any, for Nodularia is not known, but the possession of adequate supplies of the enzyme superoxide dismutase may be the key to survival under conditions of potential photo-oxidation at the lake surface (Oberley 1982).

It is not known if Nodularia behaves sim- ilarly in other saline lakes and brackish seas. Nodularia spumigena is very common in



N2fixation in Pyramid Lake 1237

Walker Lake (A = 154 km, Z = 20 m, salinity 10.50o%) which is near Pyramid Lake and is also abundant in other saline alkaline lakes throughout the world (Williams 1981). It forms N2-fixing blooms in the Baltic Sea; the most extensive work in the Baltic (Lin- dahl et al. 1980) suggests that the distribution of N2 fixation with depth is not similar to that in Pyramid Lake.

Small changes in wind speed and direc- tion control the spatially heterogeneous distribution of Nodularia biomass and nitrogen fixation. During the bloom, biomass at the surface varied by more than three orders of magnitude and N2 fixation by four orders of magnitude. A more regular pattern occurred for biomass distribution, comprising a small-scale (- 1-10 m) series of wavy stripes (Fig. 4) and large (km) curls (Fig. 5). The large-scale distribution is probably due to basin-scale advection of the buoyant algal colonies (Wrigley and Home 1974; Strong and Eadie 1978). The dominant northerly wind probably results in algal accumulations in the southern part of the lake. Since wind speeds were low during our study, Langmuir spirals are an unlikely cause of the small-scale patchiness, which is most likely due to algal clumping and convection cells. In warm, relatively high-altitude lakes, convection due to overnight cooling is an important process for vertical mixing in the epilimnion (Kittel and Richerson 1978).

Surface samples collected from throughout Pyramid Lake on any given day showed an unexpectedly poor correlation between N2 fixation and heterocyst abundance. This finding contrasts with other short term studies (Home et al. 1979; Lindahl et al. 1980; Levine and Lewis 1984), although few workers have measured such variations. However, over the whole season we found a good correlation between these two vari- ables. One explanation for the lack of short term correlation is that it is impossible to distinguish active from inactive heterocysts under the light microscope-although this might be accomplished by using transmis- sion electron microscopy or light microscopy and tetrazolium salts. The surface bloom is re-formed daily from a mixture of Nodularia filaments, some of which may be moribund. At any given time, the mere

presence of heterocysts does not indicate nitrogenase activity.

One of us (A.J.H.) has surveyed N2 fixation in lakes in four continents using 15N2 and acetylene reduction techniques. Het- erocyst-bearing algae which were not ac- tively fixing N2 at the time were common. Only when nutrients (Lean et al. 1978; Home et al. 1979), light (Lewis and Levine 1984), and turbulence are stable will heterocyst counts provide an adequate real-time estimate of N2 fixation.

Increased convective mixing of the epilimnion during October probably explains the cessation of N2 fixation in Pyramid Lake in 1979. Mixing could destroy the near-surface accumulation which is apparently es- sential to N2 fixation by Nodularia in this lake. Another reason for the decrease in N2 fixation may be a lack of soluble iron, important for N2 fixation in some lakes in semiarid zones (Elder and Home 1977; Wurtsbaugh and Home 1983). Concentra- tions of soluble iron are not known for Pyr- amid Lake. The decrease in N2 fixation was not due to any inhibition of nitrogenase activity by increases in nitrate, which had occurred by mid-November. Similar increases did not inhibit N2 fixation in other stratified lakes (Home and Fogg 1970); nitrate re- presses nitrogenase synthesis, not nitrogenase activity, in most lakes.

References ALEXANDER, V., AND D. M. SCHELL. 1973. Seasonal

and spatial distribution of nitrogen fixation in the Barrow, Alaska, tundra. Arctic Alpine Res. 5: 77- 88.

ANDERSON, H. M., AND A. J. HORNE. 1975. Remote sensing of water quality in reservoirs and lakes in semi-arid climates. Univ. Calif., Berkeley, Sanit. Eng. Res. Lab., UCB-SERL Rep. 75-1. 132 p.

ANDERSON, J. G. 1982. Breedingbiology ofthe Amer- ican white pelican in Anaho Island National Wild- life Refuge. M.A. thesis, San Francisco State Univ.

BERG, C. P., S. R. SCHNEIDER, AND D. L. GALAT. 1981. Calcium carbonate precipitation in Pyramid Lake, Nevada, as monitored by satellite: 1978 and 1980, p. 721-731. In Remote sensing of the environment. Proc. 15th Int. Symp.

CARPENTER, E. J., AND J. J. MCCARTHY. 1975. Ni- trogen fixation and uptake of combined nitroge- nous nutrients by Oscillatoria (Trichodesmium) thiebautii in the western Sargasso Sea. Limnol. Oceanogr. 20: 389-401.




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Submitted: 6 April 1983 Accepted: 6 May 1985



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Nitrogen Fixation in an Oligotrophic, Saline Desert Lake: Pyramid Lake, Nevada