Aphanizomenon ovalisporum (Forti) in Lake Kinneret ...

Journal of Plankton Research Vol.20 no.7 pp.1321-1339, 1998

Aphanizomenon ovalisporum (Forti) in Lake Kinneret, Israel U.Pollingher, O.Hadas, Y.Z.Yacobi, T.Zohary and TBerman Israel Oceanographic & Limnological Research Ltd, The Yigal Alton Kinneret Limnological Laboratory, PO Box 345, Tiberias 14102, Israel

Introduction

Over the past 30 years, cyanobacteria have been relatively minor contributors to the phytoplankton biomass in Lake Kinneret (Pollingher, 1981; Berman et al, 1992). Winter-spring blooms of Microcystis spp. were observed in the late 1960s preceding the annual bloom of the dinoflagellate Peridinium gatunense Nygaard (Pollingher, 1981,1986; Hickel and Pollingher, 1988a). Other cyanophyte species which have been occasionally recorded at high abundance in the lake phytoplankton include Chroococcus minutus (Kiitz.) Nageli in 1975, 1981 and 1984 (Pollingher, 1991), and Cyanodictyon imperfectum Cronberg et Weibull in 1973 (Hickel and Pollingher, 1988b). In general, Hormogonales were very scarce in the lake. Picocyanobacteria, mostly Synechococcus sp., have been found throughout the year, with peak abundances in summer and fall, but make only a minor contribution to total phytoplankton biomass (Malinsky-Rushansky et al, 1995). In mid-August 1994, perceptible numbers of Aphanizomenon ovalisporum Forti filaments began to appear in the lake. By early October, A.ovalisporum dominated the phytoplankton, reaching a chlorophyll concentration of -20 u.g I"1 and constituting 88% of the total biomass. The bloom declined in late October, and by mid-November no filaments remained in the epilimnetic water. This event was the first time that A.ovalisporum had been recorded in Lake Kinneret since systematic monitoring began in 1967. It marked the first appearance of a potentially toxic, nitrogen-fixing cyanobacterium in large numbers during the summer-fall season, a time of year when phytoplankton standing stocks are generally low and water utilization demands are greatest. In 1995, A.ovalisporum reappeared in July and persisted until December, but did not develop a bloom. © Oxford University Press

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Abstract. The filamentous cyanobacterium Aphanizomenon ovalisporum was observed for the first time in Lake Kinneret in August 1994 and formed a prominent bloom from September through October. Aphanizomenon ovalisporum reappeared in diminished amounts in the summer and fall of 1995. These events are the first record of significant quantities of a potentially toxic nitrogen-fixing cyanobacterium in this lake. No definite provenance of inoculum has been identified, although A.ovalisporum was also observed in a newly reflooded area (Lake Agmon) in the catchment. Unusually high water temperatures and low wind inputs were Observed prior to and during the A.ovalisporum bloom period. These, together with possibly enhanced availability of phosphorus or other growth factors, may have contributed to the cyanobacterium growth in 1994. Phosphorus limitation, as indicated by high cellular alkaline phosphatase activity, the onset of stormy conditions and a fall in water temperatures led to the demise of the 1994 bloom. Although the A.ovalisporum bloom in 1994 had no serious direct impact on water quality, the continued presence of a potentially toxic cyanobacterium in Lake Kinneret, a major national water supply source, is a cause for serious

U.PoIIingfaer el at.

The purpose of this paper is to describe the cyanobacterium A.ovalisporum and its development in Lake Kinneret in 1994 and 1995. We also provide details of the series of events of some relevant environmental parameters in an attempt to examine the causes for the appearance of this organism. Site description

Method Most of the physical and chemical data presented here are taken from the Kinneret data base. The major nutrients have been monitored routinely since 1969. Water column samples for chemical analyses and algal counts were taken weekly from 8-10 depths at a central lake station, Station A, representative of the pelagic waters. Standard methods (American Public Health Association, 1992) were used for most chemical analyses; dissolved organic nitrogen (DON) was determined by the method of Nydahl (1978). Algal biomass was quantified after preservation with Lugol's solution, 1322


Lake Kinneret is a medium-sized (170 km2) meso-eutrophic warm monomictic lake located in northern Israel at 210 m below MSL, with mean and maximum depths of 24 and 43 m, respectively. The daily net solar radiation ranges from a maximum of 24 kJ m~2 day"1 in June-July to a minimum of 1.8 kJ nr 2 day 1 on an overcast day in December. Precipitation, wind direction and velocity conform to regular seasonal patterns (Serruya, 1978). The winter overturn plays an important role in the lake metabolism. Full homothermy generally occurs between December and March, when water temperatures are between 14 and 16°C. Thermal and chemical seasonal stratification extends from April-May to mid- or the end of December. During the stratified period, the epilimnion (temperature 15-30°C) has high levels of dissolved oxygen (7.5-8.5 mg I"1), but is depleted in nitrogen (N) and phosphorus (P). The hypolimnion rapidly becomes anaerobic, with high concentrations of sulfide (5-6 mg 1~') and ammonium (NH4+; >600 ug N I"1). Throughout the year, ambient levels of soluble reactive phosphorus (SRP) in the trophogenic layer are low (1-5 jig P I"1) with a maximum of -10 ug P I"1 during the period of overturn (Berman et aL, 1997). In winter, concentrations of dissolved inorganic nitrogen (DIN) are mostly determined by the external inputs, predominantly in the form of nitrate (NO3) from the River Jordan and other streams. In addition, with overturn, NH4+ from the hypolimnion is distributed throughout the water column, and maximum trophic-zone concentrations of DIN are observed (450 ug N I"1). Thus, the levels of DIN in the epilimnion are regulated by the pattern and intensity of floods, the extent of water column mixing, by phytoplankton and bacterial uptake (Berman et aL, 1984), by zooplankton regeneration (Urabe, 1993; Sterner et aL, 1995) and by nitrification. From mid-July until November, epilimnetic concentrations of DIN are low, generally not exceeding 20-30 ug N H. The seasonal and interannual patterns of phytoplankton development have been described in detail elsewhere (Pollingher, 1981; Berman et aL, 1992).

Aphanizomenon

ovalisporum Forti in Lake Kinneret

Results Aphanizomenon ovalisporum: description of the organism The Aphanizomenon species growing in Lake Kinneret has been identified as A.ovalisporum (Figure 1). This species was first described in Lake Kutchuk Tchekmedje near Istanbul by Forti (1911) and characterized as a solitary, slightly curved blue-green trichome, 0.5-1 mm long, narrowing towards the ends, with cells 4-5 um in diameter, 1-3 times longer than they are wide (Table I). According to Forti's description, the heterocyst is globular or ellipsoid, 5-7 um in diameter and 8-12 um long. Ovate akinetes are 12-14 um in diameter and 18-20 um long. A water bloom of this organism was reported by Cannicci (1954) in Lago Albano (Italy), where the cyanobacteria were accompanied by Ceratium and a bloom of rotifers. The only other mention of A.ovalisporum in nature that we have found is a report of its presence in freshwater impoundments in Cuba by Komarek and Kovacik (1989). In Lake Kinneret, A.ovalisporum filaments were free floating, sometimes, but not always, encased in mucilage, with one or a few terminal hyaline cells (Figure 1). The filaments were shorter (25-400 mm) and thinner (3-4 u,m, very rarely 5 urn in diameter) than those described by Forti (1911). The length of the cells was not always well defined and varied between 5 and 10 um; the terminal hyaline cells were longer. At the end of the bloom, older filaments developed terminal segments of elongated colorless cells. The heterocysts and akinetes were also smaller than those reported by Forti. The spherical heterocysts, 3-5 um in diameter, were usually located in the middle of the trichome, but also occasionally at the tip. Akinetes were 5-10 um in diameter and 7-15 um long, located in the middle of the trichome, very rarely adjacent to the heterocyst, and sometimes also 1323


sedimentation and counting with a Wild inverted microscope using Utermohl's method (1958). The determination of A.ovalisporum biomass was based on the measured volume of the filaments. The total tissue volume was expressed as 106 jim31"1, equal to ug I"1 or mg nr 3 , based on the assumption that the specific gravity of the cyanobacterium is one. The cumulative length of the filaments was expressed as m I"1 (meters of filament per liter) (Bailey-Watts et al., 1987). Heterocysts and akinetes were counted and expressed as the number of heterocysts and akinetes per 1000 um filaments (Ogawa and Carr, 1969). Chlorophyll concentrations were determined by fluorescence after acetone extraction (Holm-Hansen etai, 1965) and primary production was measured with a modified version of the H14CO3 uptake method (Steemann Nielsen, 1952). Alkaline phosphatase activity was measured from the increase in fluorescence, when 4-methylumbelliferyl phosphate (MU-FP) substrate (Sigma) was hydrolyzed to give the highly fluorescent product 4-methylumbelliferone (MU) (Hoppe, 1983). Monoalgal batch cultures of A.ovalisporum isolated from Lake Kinneret were grown on several media, differing in their nutrient content. These were blue green (BG) medium (Moss, 1972), Lindstrom medium (Lindstrom, 1983) and artificial Kinneret water (AKW).

UPoUingher et al.

at a terminal position. The distance between heterocysts and akinetes varied from 20 to 60 um, rarely 90-120 um. When grown in the nutrient-rich BG medium, A.ovalisporum isolated from Lake Kinneret developed longer filaments and larger heterocysts and akinetes than the natural populations. In these cultures, the cells were 2-5 um in diameter and 5-8 um long; heterocyst diameter was 5 urn (Table I). The akinetes were 8-10 Um in diameter and 15-20 um long. When inorganic N was excluded from the medium, most of the trichomes had three heterocysts and three akinetes, and in most cases the akinetes were adjacent to the heterocysts. When grown on AKW or Lindstrom medium, in which the concentrations of nutrients are lower than in BG medium, the cyanobacterial filaments resembled those from the lake. In AKW with no added N, the trichomes developed only a single heterocyst and, rarely, one akinete. Even when growing in AKW or Lindstrom media with either inorganic (NH», NO3) or with organic N substrates (e.g. 1324


Fig. 1. Aphanizomenon ovalisporum:filamentsshowing heterocysts and akinetes. Bar = 10 mm.

Aphanizomcnon ovalisporum Forti in Lake Kinneret Table L Aphanizomenon ovalisporum Forti dimensions (in um)

Trichome Cells Heterocyst, globular Heterocyst, ellipsoidal Akinete

Length Diameter Length Diameter Diameter Length Diameter Length

Forti 1911

Lake Kinneret

BG medium

500-1000 4-5 4-12 5-7 8 12 12-14 18-20

25^00

25-600 2-5 5-8 5 8 12 8-10 15-20

5-10 3-5 5-10 7-15

urea, hypoxanthine, guanine, lysine), trichomes bearing heterocysts and akinetes were observed (Berman, 1997). Phytoplankton development in Lake Kinneret, 1994 and 1995

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Lake Kinneret phytoplankton populations are usually dominated by a diverse assemblage of dinoflagellates in late winter-spring and by Chlorophyta supplemented by diatoms and cyanobacteria during summer and fall. The contribution of cyanobacteria to the total phytoplankton biomass is generally small (the annual average from 1969 to 1993 ranged be-tween 6 m s"1) during 1994 and 1995 with the multi-annual (1988 through 1993) monthly average (Figure 4). In general, most months of 1994

25 20

o

A

1994 1993

man 1970-93

A X\sA

/ n

.1 CO

•—

\

°A

6 Aug

Sep

Oct

Nov 1

Fig. 3. Changes with time in chlorophyll concentrations (ug h averaged for the euphotic zone) in Lake Kinneret, August through November 1993 and 1994 in comparison with the multi-annual mean (1970-1993).

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Rates of photosynthetic carbon fixation during the A.ovalisporum bloom from 12 September until the end of October 1994 were unusually high in comparison to those normally observed during this season (1.6- to 2-fold the multi-year average; Table IV). The elevated rates of photosynthetic activity may not have been due entirely to A.ovalisporum because unusually high numbers of Peridiniopsis spp. were also present in the phytoplankton (see above). We have no data on the specific photosynthetic activities associated with A.ovalisporum and Peridiniopsis. The values of assimilation numbers (ranging from 3.62 to 6.5 mg C mg"1 Chi h"1 at optimum depth) during the A.ovalisporum bloom were also significantly higher than those normally observed in Lake Kinneret at this time (Table III). Highest assimilation numbers were observed at the beginning of the bloom, and declined over the duration of the bloom. Correspondingly, carbon turnover times were short at the beginning of the bloom (0.8 days), increasing to 6 days in November (Table IV). The levels of primary production were again significantly above the multi-year average throughout the summer-fall of 1995.

Aphanizomenon ovalisporum Forti in Lake Kinneret £ 200

J_M.M.J.S_N_J_M.M.J.S_N F A J A O D F A J A O D

Fig. 4. The wind regime in Lake Kinneret, 1994-1995, in comparison with the multi-annual mean. Data shown as monthly total hours of wind >6mr'. Vertical bars are standard deviations of the multiannual means. Table VI. Monthly averages of epilimnetic water temperatures in Lake Kinneret during 1994,1995 in comparison with the multi-annual monthly averages

Jan. Feb. March April May June July Aug. Sep. Oct. Nov. Dec.

1969-1993

1994

1995

°C

+SD

°C

°C

15.6 4.9 15.6 18.3 21.6 24.8 26.9 27.9 27.7 25.9 22.3 18.3

16.6 15.8 16.9 19.4 22.8 25.9 27.7 28.5 28.4 26.9 23.8 19.6

16.8 15.9 16.2 18.8 22.6 25.2 27.3 28.0 28.8 28.6 23.0 17.8

15.9 15.6 17.3 18.6 23.0 26.4 27.9 28.7 28.1 25.9 22.8 17.6


Month

had fewer hours of strong wind than the corresponding long-term average, notably in February, March and October 1994. Again in 1995, from January through May and in September-October, the winds were exceptionally subdued. Monthly averages of trophogenic layer temperatures (0-10 m depth) in 1994 and 1995 were compared to the long-term (1969-1993) averages (Table VI). Throughout 1994, water temperature was somewhat warmer than the long-term average in winter, spring and fall, but not during the months June-August. Note, however, that epilimnetic water temperatures for September-October 1994 were significantly warmer than either the multi-year average or the temperatures in September-October 1995. Patterns of nitrogen and phosphorus in lake waters in 1994 and 1995 In Figure 5, the monthly average concentrations of DIN measured in the epilimnion of Lake Kinneret from January 1994 through December 1995 are compared with the long-term (1969-1993) monthly averages of these parameters. 1333

UJtoDmgher et al.

J

M F

AMJJASONDJFMAMJJASOND 1994

1995

Fig. 5. Average monthly concentrations of DIN (mg N H ) , 0-10 m depth, 1994 and 1993. Also shown are multi-annual monthly averages with standard deviations (vertical bars). Measurements at a central station, A.

0.4

•

I" 0.2

•

lllll

Q 0.1 •

i

i i

mean 1983-91 1994-95

0.0

'

J

FMAMJJASONDJFMAMJJASOND 1994

1995

Fig. 6. Average monthly concentrations of DON (mg N H ) , 0-10 m depth, 1994 and 1995. Also shown are multi-annual monthly averages with standard deviations (vertical bars). Measurements at a central station, A.

The concentrations of DIN from January until July 1994 tended to be below the multi-annual average; from August through October, these were close to the low ambient levels usually observed in the lake at this season. Concentrations of DIN rose above the multi-year average in November 1994 and remained high until June 1996. DON concentrations in the epilimnetic waters during 1994 and 1995 showed much greater variability than the multi-year monthly averaged values (Figure 6). An increase in DON concentrations from June through the beginning of September 1994 was followed by a sharp fall, concomitant with the development of the A.ovalisporum bloom. At the end of the cyanobacterial bloom, DON concentrations rose again and remained high until March-May 1995, before falling steadily throughout the remainder of 1995. Available P concentrations, here shown as total dissolved phosphorus (TDP) (Figure 7), were somewhat below the multi-annual averages at the beginning of 1994, increased to a slightly higher than average value in July and August, and then fell sharply with the development of the cyanobacteria in September. After the termination of the bloom, TOP concentrations rose again before decreasing 1334
