Journal of Plankton Research Vol.10 no.5 pp.921-939. 1988
Primary and bacterial production compared to growth and foodrequirements of Daphnia longispina in Lake Kvernavatnet, westNorway
Knut Yngve B0rsheim, Sissel Andersen, Geir Helge Johnsen1, Eva 0enKambestad1 and Svein NorlandUniversity of Bergen, Department of Microbiology and Plant Physiology, Alligt.70, N-5000 Bergen and' University of Bergen, Department of Animal Ecology,Museum of Zoology, Musiplass3, Bergen, Norway
Abstract. Primary production, and bacterial production as measured by incorporation of [3H-methyljthymidine into ice cold TCA insoluble material were investigated during 1984 in LakeKvernavatnet, west Norway. Primary production averaged 222 mg C m~2 day . and bacterialproduction averaged 163 mg C m~2 day"1. The bacterial production in the euphotic pelagic zonecontributed ~60% of the total pelagic bacterial production. The zooplankton was dominated byDaphnia longispina. From growth experiments with animals fed only natural food in coarse filteredlake water, the population daily growth increments were calculated. The average production ofD.longispina was 151 mg C m~2 day"1 during the period investigated. The estimated primaryproduction was too low to sustain both the bacterial production and the zooplankton foodrequirements. These results imply that the carbon cycle of the lake is dependent on the supply ofallochtonous material, or that the current methods for measuring production rates in aquaticenvironments are systematical erratic.
Introduction
In plankton ecology, recent progress has been made by multidisciplinaryprograms for the study of processes including a more expanded range oftaxonomic groups than can be handled by individual experts. Such efforts areproviding insight into the quantitative importance of the various parts of thefood web in various environments. Frequently it is difficult to compare studiesfrom older literature because the most convenient units such as number ofindividuals, length or size of body have been used. A modern approach forcesthe individual worker to aim at a common unit of comparison.
In the investigation reported here, we measured rate processes and biomassesof the dominating parts of the carbon cycle in a humic, slightly eutrophic lake.We converted production rates and biomasses of phytoplankton, bacteria andthe dominating crustacean zooplankton into carbon units to facilitate com-parison among these parts of the food web of the lake.
Primary production has been used as an indicator of productivity in lakes for along time. However, bacterial secondary production may also be an importantproduction process in aquatic ecosystems (Azam et al., 1983). Recent develop-ments of methods for measuring bacterial production have stimulated researchon the in situ growth rate of bacteria (Hagstrom et al., 1979; Karl, 1979;Fuhrman and Azam, 1980, 1982). Reports from a variety of environments haveshown that aquatic bacteria occasionally are more important as producers ofpaniculate organic material than previously believed (Pedr6s-Ali6 and Brock,
1982; Riemann, 1983; Bell etal., 1983; Bell and Kuparinen, 1984; Lovell andKonopka, 1985; Murray and Hodson, 1985; Scavia etal., 1986). In other studies,bacterial production was found to be only 5-10% of the primary production(Riemann et al., 1982; Kirchman et al., 1984).
To quantify the importance of bacterial production in the carbon cycle of thelake we studied, we measured bacterial production with the [3H]thymidinemethod (Fuhrman and Azam, 1982; Riemann et al., 1982). Bacterial total countand bacterial mean cell volume was measured in the same samples. These resultswere compared with measurements of primary production rates.
There is increasing evidence that both primary and bacterial secondaryproduction in pelagic ecosystems are harvested by grazers. In eutrophic lakes,cladocerans have been shown to ingest both algae and bacteria (Peterson et al.,1978; Bogdan and Gilbert, 1982; DeMott, 1982; B0rsheim and Olsen, 1984),and at their maximum abundance they are at times able to graze downphytoplankton, thereby depleting their own food sources (Lampert et al., 1986;Sommer et al., 1986). In Lake Kvernavatnet the crustacean zooplankton isdominated by the cladoceran Daphnia longispina. We measured the biomassand daily growth increment of this species. The food consumption of a majorpart of the zooplankton could then be compared to the primary and the bacterialproduction during the year 1984.
Materials and methods
Lake Kvernavatnet is situated on the west coast of Norway (60°6'N, 5°14'E).The maximum depth is 30 m, the mean depth is 12.5 m and the area is0.125 km2. The lake is used for aquaculture purposes, and ~300 000 fingerlingsof salmon are reared annually in net pens. The daily input of dry fish feed to thesalmon during the period investigated was 60 kg day"1. The fish farm wassituated 100 m south of the sampling station.
Samples were taken from the deepest part of the lake with a 1.6 1 Ruttnersampler. The water samples were always shaded from direct sunlight andprocessed within 5 min. Subsamples for estimation of phytoplankton biomasswere preserved with Lugol's blue and later counted in the inverted microscopeafter sedimentation (Utermohl, 1958). Cell sizes of the dominating species weremeasured to the nearest 1 \im and cell volumes were calculated using simplegeometrical models. Cell carbon was calculated using 100 fg C fim~3 (Strath-mann, 1967). Since the same factor was used for all groups, the volume of thecell types that shrink during fixation may have been underestimated by as muchas a factor of two (B0rsheim and Bratbak, 1987).
Primary production was measured with the [14C]CO2 light and dark bottleincubation method (Steeman Nielsen, 1952). Replicate samples in 125 mltransparent and black bottles were dosed with 5 \x.C\ [14C]NaHCO3 (NewEngland Nuclear). The bottles were incubated in situ for 2 h. After incubationthe bottles were kept in the dark and 25 ml subsamples were filtered on 0.2 u.mpore size Nuclepore filters within 20 min. Radioactivity on the filters weremeasured with liquid scintillation counting using Safefluor* (Lumac, Belgium)as scintillation cocktail and the channels ratio method for quench correction.
Production compared to requirements of D.kngispina
Incident light was measured with an Li Cor 190SB Quantum Sensor connectedto an integrating recorder (LI-COR Ltd, NE, USA). The time integrated lightmeasurements were recorded every 10 min during the incubation of the primaryproduction experiments, and every hour during the rest of the periodinvestigated.
Concentrations of inorganic carbonates were measured with a CO2 gasanalyser (The Analytical Company Ltd, type 225 HK2) as described byB0rsheim and Andersen (1987).
Daily primary production was calculated as:
Pd = (Pi x /;)//„
where Pd is daily primary production, Pj is the primary production during theincubation, /j is the integrated light during the incubation and /d is the integratedlight for the day.
Subsamples for estimation of bacterial biomass were preserved with 2%glutardealdehyde (final concentration). Total numbers of bacteria were countedwith epifluorescence microscopy after staining with acridine orange (Hobbie etal., 1977). Sizes of bacterial cells were measured in the same preparations usingan eyepiece graticule (Bratbak, 1985). The measurements were calibrated withmonodispersed fluorescent particles (B0rsheim, 1984). The lengths and widthsof more than 25 bacterial cells were measured in each preparation. Cell volumewas calculated as W2(L - W/3)TT/4, where W is the width and L is the length ofthe bacterial cell. Bacterial dry wt was calculated from volume estimates using320 fg dry wt u.m~3 as suggested by Bakken and Olsen (1983), and carbon wasassumed to be 50% of the dry wt.
Thymidine incorporation was measured according to Fuhrman and Azam(1982), with modifications suggested by Riemann et al. (1982) and Riemann(1984). Samples in 60 ml sterile transparent bottles were added [3H-methyl]thymidine (New England Nuclear) to a final concentration of 12.5 nmol I"1, andincubated in situ. Samples from the epilimnion were incubated for 15 and 30min, and samples from the hypolimnion were incubated for 30 and 60 min. Theincubations were terminated by adding formaldehyde (2% final concentration).Time series showed that the incorporation was linear with time for >30 min inthe epilimnion and for >60 min in the hypolimnion.
Subsamples (3 ml) were filtered within 2 h on 0.2 \x.m pore size Nucleporefilters, and washed three times with 3 ml of ice cold, 5% TCA. The filters weretransferred to scintillation vials, and dissolved in Lumasolve® (Lumac, Belgium).Lipoluma® (Lumac, Belgium) was used as scintillation cocktail and quenchingwas corrected for with the channels ratio method. The estimate of incorporationrate was calculated as the mean rate from the two incubation times. Thymidineincorporation rate was converted to cell production assuming 2.1 x 1018
bacterial cells were produced per mol thymidine incorporated (Fuhrman andAzam, 1982; Bell et al., 1983; Riemann, 1984).
Zooplankton samples were taken with a 28.5 1 modified Schindler/Patalastrap. Three replicate vertical series were taken, and the samples were preserved
in 4% formaldehyde with 10% sucrose (Haney and Hall, 1973). The number ofD.longispina and the number of eggs per individual were recorded for eachsample. The body length of 60 randomly chosen individuals was measured to thenearest 30 u,m.
The relation between length and biomass of D.longispina was measured onceduring the period investigated (29 June 1984). Living D.longispina wereanaesthetized with carbonated lake water, measured at x40 magnification andtransferred to Sn-capsules for carbon analysis. Non-ovigerous females wereselected. Single specimens were analysed only for the largest sizes, whereas forthe smaller sizes several individuals of similar size were pooled in each capsula.As many as 50 specimens were needed for reliable chemical analysis of thesmallest sizes. Carbon was measured in a Carlo Erba Elemental Analyzer Mod-1106.
The relation between body length and carbon content is shown in Figure 1. Alog-log linear regression of the results is given by equation:
C = 2.507L2 59° (1)
where C is u.g carbon, and L is length in mm (r = 0.972, n = 36).Somatic growth rates of D.longispina were measured with 'in situ' growth
experiments as described by Larsson et al. (1985). Cohorts of D.longispina werereared in flow through chambers in the absence of predation. The animals werefed only coarse filtered water from 1 m depth in the lake throughout their lifecycle. These experiments were carried out four times during the periodinvestigated.
15 mm
Fig. 1. The relation between carapace length and carbon content of Daphnia longispina from LakeKvemavatnet.
Production compared to requirements of D.longispina
The relation between size and age can be given as:
L = aebA (2)
where L is length (mm), A is age (days), and a and b are constants estimatedfrom the results of the growth experiments.
The age-length relationship was then applied to the results from the biomassmeasurements of the lake zooplankton. Using equation (2), the age of eachmeasured individual could be calculated. Then, from the same equation, thelength of the same animal after a 24 h growth period could be calculated byincreasing the age by unity. The lengths were converted to carbon usingequation (1), and the growth increments were calculated by subtracting themeasured biomass from the estimated biomass 24 h later.
This procedure was applied to all individuals measured, summed up andintegrated for the whole lake using the total count measurements.
The reproductive part of growth was calculated from birth rates estimatedfrom observed egg numbers, egg development times and observed length ofneonates. Total daily production was calculated as the sum of somatic growthand reproduction.
Results
Primary production and phytoplankton biomass
Primary production increased during April and May to a maximum in thebeginning of June followed by a dramatic decrease (Figure 2). Two subsequentmaxima were observed, in July and in August.
The phytoplankton biomass followed a pattern similar to primary production(Figure 3). The spring bloom was dominated by cryptomonads and smalldiatoms, and the peak in July was dominated by green algae (Ankistrodesmusjudai) and cryptomonads (Figure 4). The peaks in August and September weredominated by various cryptomonads.
The annual primary production was 45 g C m~2. As shown in Figure 5, theeuphotic zone only reached down to 4-4.5 m. The extinction coefficient of lightin the water column was 0.91 m"1, as measured with a submersible light sensor(Johnsen and Jakobsen, 1987). The low transparency is caused by highconcentration of humic substances, and may explain the shallow euphotic zoneand the relatively low annual primary production.
Bacterial production and biomass
Bacterial production as measured with the thymidine incorporation methodincreased during the spring bloom, following a pattern similar to the primaryproduction. The decline in the middle of June reduced the bacterial productionby a factor of 2, whereas the primary production was reduced by a factor of 8(Figure 2). After that, a second maximum in total bacterial production wasobserved in the beginning of July.
Fig. 2. Production rates of phytoplankton, bacteria and Daphnia longispina during 1984 in LakeKvernavatnet.
The depth profiles of [3H]thymidine incorporation rates are shown in Figure6. The highest values were measured above the thermocline. Below thethermocline, the incorporation rates were generally lower, in the range0.67-3.6 pmol [3H]thymidine incorporated I"1 h~\ except in September whenone value of 14 pmol I"1 h"1 was measured at 18 m.
As shown in Figure 5, the euphotic zone was only 4-4.5 m deep, but high
Production compared to requirements of D.longispina
2J0
1,5
1,0
CM
EO 0n 1,0
OS
25
2J0
1,5
05
DAPHNIA L0NGISP1NA
110MAY JUN JUL AUG SEP
Fig. 3. Depth integrated biomass of phytoplankton, bacteria and Daphnia longispina during 1984 inLake Kvemavatnet.
[3H]thymidine incorporation rates were usually found at all depths above thethermocline, down to 8-9 m (Figure 6). In September, [3H]thymidine incorpor-ation rate increased with depth down to the thermocline. Profiles of [3H]thy-midine incorporation rates and bacterial total count did not follow similarpatterns (Figures 6 and 7). On May 22, both [3H]thymidine incorporation ratesand total count decreased steadily with increasing depth. On June 21 there was apeak in bacterial total count in the thermocline, but the [3H]thymidineincorporation rate in the sample was low. On June 21, the total count and the
Fig. 4. Some depth profiles of phytoplankton biomass. R: Rhodomonas sp ; D: diatoms; Cm:Cryptomonas marssonii; G: green algae; C: cryptomonads; M: Mallomonas sp.
[3H]thymidine incorporation rate profiles showed reverse trends down to thethermocline, with [3H]thymidine incorporation rates decreasing with depth, andtotal count increasing with a peak in the thermocline. The two next samplingdays the two bacterial parameters showed more similar patterns, and inSeptember both [3H]thymidine incorporation rates and bacterial total count hada peak in the thermocline.
Production compared to requirements of D.longispina
PHYTOPLANKTON BIOMASS, mm3 liter-1
0 2 4 6 0 2 4 6
R . > DP" °
\ \ :
14 May • 1 7 Jun •
13 Jun
N.76O6
•-0507
Jun/Jul -
0 2 4 6 0 2 4 6
6 •17
10 Jul -/
18 Jul •
0 2 4 6 0 2 4 6
7 Aug • 14 Aug •
(o
2
4
6
8
) 2 4 6
28 Aug •
() 2
• )
• /
4 6
25 Sep •
Fig. 5. Some depth profiles of primary production rates in Lake Kvemavatnet.
A correlation analysis of the bacterial parameters showed that thymidineincorporation was correlated with water temperature and primary production(99% level of significance), and with bacterial mean cell volume (95% level ofsignificance). Thymidine incorporation rate and bacterial total count were notcorrelated.
Fig. 6. Thymidine incorporation rates (filled squares), compared to temperature (open circles) inLake Kvernavatnet during 1984.
Daphnia longispina biomass and production
Biomass of D.longispina was calculated from numbers and length measure-ments, and integrated for the whole water column (Figure 3). The total biomassincreased steadily during the summer, reaching a maximum in late July, andthen decreased drastically from July 17 to July 24.
Fig. 7. Depth profiles of bacteria biomass in Lake Kvernavatnet during 1984.
The results from the growth experiments in flow through chambers are shownin Table I as regression equations of length versus age. The depth integratedgrowth rates calculated from these results are shown in Figure 2, and somedetails of the calculations are shown in Table II.
Measurements of egg numbers per individual and brood size showed thathighest brood sizes occurred in June, followed by a decline in late June and anew maximum in late July (Table III).
In the beginning of June, when the phytoplankton and the bacterialproduction declined, the D.longispina population were concentrated in theeuphotic zone (Figure 8). The biomass and production of phytoplankton werealso located in the upper 4 m (Figures 4 and 5) and the distribution of thezooplankton suggest that during the spring bloom harvesting of the phytoplank-ton takes place in the euphotic zone. Later, when food became more sparse, thedistribution of the D.longispina population became more complex (Figure 8).The peaks in the D.longispina biomass below the thermocline from June 18 andlater, consisted mainly of juveniles. The majority of the adults were still found inthe euphotic zone, during both day and night (Johnsen and Jakobsen, 1987).
Table I. The relation between animal size, age and growth rate during four in situ growthexperiments in Lake Kvernavatnet
Experimental period a b r* n"
30 May-13 June21 June-4 July12 July-25 July23 August-9 September
0.66820.70670.73180.8782
0.08210.05010.05610.0382
0.890.930.910.80
79121198
19
The values have been calculated from semi-logarithmic linear regressions (equation 2).•Correlation coefficient.**Number of measurements.
Table U. D.longispwa biomass and growth in Lake Kvernavatnet during 1984
Day
22 May29 May
5 June12 June18 June26 June
3 July12 July17 July24 July14 August24 August
Table HI.
Date
18 June26 June
3 July12 July17 July
Number(Individuals
8.8 x 103
2.9 x 104
1.1 x 103
9.7 x Iff1
3.0 x 105
3.5 x 105
2.2 x 1O3
2.0 x 103
3.7 x 105
5.4 x 104
6.4 x 10*6.7 x 1CT*
Brood size and
Reproductive growthm"2) (mg C m"2 day"1)
0.6653.6868.1579.084
55.112.013
20.1850.59
140.09.991
13.774.924
egg number of D.longispina in
Brood size
4.311.633.743.303.76
Somatic growth(mg C i r r 3 day"1)
5.87123.2394.2862.13
209.0121.9146.3214.6416.2
50.2431.2728.21
Lake Kvernavatnet
Total production(mg C m ' 3 day"1)
6.4626.92
102.471.22
264.1215.0167.1265.2556.160.2345.0433.13
during 1984
Eggs per individual
1.100.040.701.381.37
Discussion
Many studies of food web interactions are presently using carbon as a commonunit. The energetic value of a step in a food chain depends on more than thecarbon content of the prey, such as the exact reduced state of the carbon, theedibility or availability of a certain prey. Therefore, when perfection of food webstudies are called for, refinements will be necessary. At the present state of theart, carbon content of individual members of the food web and transfer rates ofcarbon is the most reasonable choice of a common unit of comparison among thedifferent parts of the food web.
Production compared to requirements of D.longispina
0
5
10
«
20
25
0
5
«
0 30 K> 90 120 0 3 0 6 0 9 0 1 2 0
? :12Jun .
1 ' ' 1,1
. / «Jun .
/ . . . .0 3 0 6 0 9 0 1 2 0 0 3 0 6 0 9 0 1 2 0
. / 26Jun .
~# •
• —
I 3 Jul ./ . . . ,
0 300090120 0 300090120
0
5
10
•a
20
25
0 306090120 0 306090120
}'\ :
HAug .
0 3 0 6 0 9 0 1 2 0 0 3 0 6 0 9 0 120
pg Daphnlal
Fig. 8. Depth profiles of Daphnia longispina in Lake Kvernavatnet during 1984.
Primary production
The average primary production during the period studied was 222 mg C m~2
day"1. In addition to the production of particulate material, algae may release apart of their photosynthetized products as dissolved exudates, and this releasehas been found to be in the range 5-45% of the total production (S0ndergaard etal., 1985). They found a mean release of dissolved organic material of 21% ofthe total carbon fixed in four Danish lakes. They also showed that this release isimmediately utilized by the bacteria. However, even if the exudation were in the
upper range of the values reported by Sendergaard et al. (1985), or referencestherein, it would not be sufficient to sustain the bacterial production in LakeKvernavatnet. As will be discussed below, the primary production is smallcompared to the consumption of organic material in the lake ecosystem. It hasbeen shown that incubation procedures sometimes underestimate primaryproduction because activity may be inhibited by toxic contaminants introducedby equipment (Fitzwater et al., 1982), and also because cells may break duringfiltering after the incubation. We used carefully cleaned glassware, avoideddirect sunlight when adding the isotope, and vacuum below 200 mm Hg duringfiltration. Even with these precautions, there is still the possibility thatincubation procedures lead to underestimates of production rates (Fitzwater etal., 1982).
The primary production varied through the year in a typical pattern fordimictic lakes in temperate climates (Sommer et al., 1986). After the springbloom from April through May, both primary production and phytoplanktonbiomass decreased drastically. The resulting 'clear water phase' in June is acommon phenomenon, and has been attributed to heavy grazing pressure fromcladocerans (Lampert et al., 1986; Sommer et al., 1986). The annual primaryproduction places Lake Kvernavatnet among the mesotrophic lakes, the patternof phytoplankton and zooplankton successions being intermediate compared tothe oligotrophic and eutrophic lakes discussed by Sommer et al. (1986). In LakeKvernavatnet the phytoplankton decline was not associated with the highestzooplankton biomass in the season studied. In the beginning of June, productionof D.longispina was —240 mg C m~2 day"1, and the maximum primaryproduction was 304 mg C m~2 day"1. It is therefore not unlikely that thephytoplankton bloom was grazed down at the point when the zooplanktonbiomass reached a critical level. The subsequent oscillations may also beinfluenced by the high grazing pressure. The first bloom after the decline in Juneconsists of a green algae that may be suspected to have small nutritive value forD.longispina, and after the decline in zooplankton the highly nutritivecryptomonads increased to an autumn maximum.
Bacteria
Methodological considerations. There is increasing evidence available that[3H]thymidine incorporation rate is a valid indicator of bacterial growth rate inaquatic ecosystems (Fuhrman and Azam, 1982; Kirchman et al., 1982; Bell et al.,1983; Scavia et al., 1986). However, the conversion from thymidine incorpor-ation rate to bacterial production in terms of cell number or bacterial carbon is aproblem. Fuhrman and Azam (1980) derived a theoretical conversion factor forcalculating production of bacterial cells from thymidine incorporation rates.Later they presented empirical evidence for the conversion factor (Fuhrman andAzam, 1982). Since we did not have the capacity to measure a site-specificconversion factor, one from the literature had to be chosen. We calculated thebacterial production rate from thymidine incorporation rate using the con-version factor suggested by Fuhrman and Azam (1982). This makes our estimate
Production compared to requirements of D.longispina
conservative, and comparable to most of the available literature when* the[3H]thymidine incorporation method has been used. We are aware that theabsolute values may have to be revised in the future, according to evidence fromlakes of comparable physical, chemical and microbiological composition.
An estimate of average cell carbon content is needed to calculate productionof bacterial carbon (Fuhrman and Azam, 1982; Kirchman et al., 1982; Bell et al.,1983; Bell and Kuparinen, 1984; Scavia et al., 1986). Conversion factors from 90to 560 fg C urn"1 have been suggested to convert bacterial measured volumesinto carbon (Nagata, 1986). Earlier values from Lake Kvernavatnet have beencalculated using the conversion factor of Bakken and Olsen (1983), andassuming that carbon constitutes 50% of the dry wt (Btfrsheim, 1984). We feelthat the conversion factor we used earlier is still not invalidated, but futureevidence may lead to a revision of the values for cell volume to cell carbonconversion factors (Bj0rnsen, 1986a; B0rsheim and Bratbak, 1987; Lee andFuhrman, 1987; Norland et al., 1987).
Bacterial production and biomass. The spring bloom of phytoplankton wasparalleled by an increase in bacterial activity, and both bacterial number andbacterial production increased during spring. A similar coupling betweenbacteria and phytoplankton during the spring bloom has been demonstrated inLake Erken, Sweden (Bell and Kuparinen, 1984). A maximum in bacterialproduction was reached in the beginning of June, followed by a mid-summerdepression, which was less pronounced than the decrease in primary production.The decrease in bacterial production may be a consequence of lower directavailable exudates from the phytoplankton, or of increased grazing pressure. Adecrease in bacterial biomass coinciding with the decline in phytoplankton, andhigh grazing pressure has earlier been reported by Kato (1985).
Few investigators have considered relations between bacterial productivityand environmental factors. Pedr6s-Ali6 and Brock (1982) and Murray andHodson (1985) found a surprisingly high correlation between bacterial pro-duction rate and water temperature. In Lake Kvernavatnet, temperature alsowas correlated with thymidine incorporation rate. From the temperature versusthymidine incorporation relation, a Q10 of 4.7 can be calculated. This value ishigher than is usually observed for pure cultures of bacteria, suggesting that thedifferent bacterial populations at the various depths in the lake are adapted todifferent temperatures.
Bacterial mean cell volumes were also correlated with thymidine incorpor-ation rate. It has been suggested that bacteria may respond to nutrient limitationby producing smaller cells (Pomeroy, 1984). Our observations do not contradictthis hypothesis since larger mean bacterial volumes were associated with higherthymidine incorporation rates. Smaller mean size was also associated with higherdepth.
For practical reasons, primary and bacterial production were not measured onthe same days. When they are compared on the occasions when they weremeasured on almost adjacent dates, the ratio between bacterial and primaryproduction spans from 0.2 to 3 (Table IV). Right after the collapse of the spring
Table IV. The ratio between the depth integrated bacterial and primary production
Date of measurementBacterial production
April 28May 22June 5June 14June 21June 27July 9August 8September 12
Primary production
April 30May 14May 23June 7June 13June 26July 7August 7September 25
Ratio:bacterial productionprimary production
0.200.580.580.251.522.043.250.620.73
bloom, the bacterial production was higher than the primary production, and onJuly 7 the maximum ratio was measured.
In Lake Kvernavatnet bacterial production was equal to the gross primaryproduction on the average. It is frequently assumed that the growth substratesfor the bacteria come from the primary producers. To sustain a given netproduction at least twice as much organic material must be consumed as isproduced by the bacteria (Bell and Kuparinen, 1984), and recent evidencesuggests that five times the net bacterial production is needed (Bj0rnsen,1986b). In addition, our estimate of bacterial production is on the conservativeside. That means that the bacteria in Lake Kvernavatnet consume an amount ofcarbon at least equal to twice the primary production and possibly five times theprimary production. The fact that the influent of the lake is rich in humus (lakewater pt = 60), which may be a substrate for the bacteria in the lake, mayexplain the high secondary production compared to the primary production. Thecommercial feeding of juvenile salmon in net pens also introduces allochtonousorganic material, at a rate of 500 mg fodder m~2 day"1. At least 20% of thismaterial is eaten by the salmon, and an additional but unknown amount is eatenby wild fish. The fodder is designed to sink before it is dissolved, but it is possiblethat the introduction of the salmon breeding net pens has changed the carboncycle of the lake to a more saprobiation-based food web. However, we believethat such a change would be followed by a change in the structure of thezooplankton and phytoplankton. The zooplankton have been observed from1982 to 1986, and have not changed much during this period. The phytoplank-ton, however, seem to reflect a transient stage of development between a meso-and eutrophic situation.
High bacterial production rate compared to primary production has beenfound in other aquatic ecosystems but not as high as in Lake Kvernavatnet.Pedr6s-Alli6 and Brock (1982) found a daily production rate of 0.1-2.5 g C m~2
with FDC and [35S]SO4 uptake measurements in Lake Michigan. There wasproduced 100-200 g bacterial carbon year"1, which was 50% of the primaryproduction. Lovell and Konopka (1985) found that bacterial production
Production compared to requirements of D.longispina
averaged ~44% of primary production in two dimictic Indiana lakes with similarwater chemistry and different productivity. In Lake Kvernavatnet the mean was109% during the period we investigated.
Daphnia longispina production
Maximum D.longispina abundance occurred ~4 weeks after the maximum inbacteria and phytoplankton (Figure 3). The production of D.longispina was151 mg C m~2 day"1 on average during the period investigated. During the sameperiod, the primary production averaged 222 mg C m~2 day"1. The bacterialproduction was 163 mg C m~2 day"1 on average. Part of the bacterialproduction is available to D.longispina (B0rsheim and Andersen, 1987). Part ofboth primary and bacterial production is eaten by other members of the foodweb in Lake Kvernavatnet, such as ciliates and other cladocerans (B0rsheim,1984).
Daphnia converts food into growth with an efficiency of ~10% during most oftheir life cycle (Richman, 1958; Kersting, 1978; Lynch et al., 1986). Thus theyconsumed ~15O0 mg C m~2 day"1 on average during the period we investigated.The sum of the primary and bacterial production was only 385 mg C m~2 day"1.Even if a minimum estimate of D.longispina growth is used, the measuredproduction of paniculate material is low compared to the animals foodrequirements. During the period from May 22 to July 17 the biomass ofD.longispina increased from 25 mg C m~2 day"1 to 2998 mg C m"2 day"1,which implies an average net production of 65 mg C m"2 day"1. Consequently,they consumed ~650 mg C m"2 day"1 on average during this period. Of course,it is possible that they did not consume so much at the end of the period but werestarving, having a lower food consumption than we assume. However, this canonly have been important at the end of July, before the population breakdown,because before that the animals grew and reproduced, and therefore must haveconsumed food. However, egg number and brood size show marked decreasefrom the beginning of June, implying that food had become limiting for growthand production.
Conclusion
During the summer of 1984, the primary production as measured by the[14C]CO2 incubation technique was too low to provide enough substrate both forthe bacterial production and the food requirements of the D.longispinapopulation. In addition, the rest of the zooplankton would represent anunknown but presumably significant consumption of primary and bacterialproduction. Since the fish breeding plant is only 100 m away from the samplingstation, the fish fodder may contribute a significant portion of the unexplainedfood requirement. The bacterial production, which may also consume anamount of carbon exceeding the total primary production, may also bestimulated by the fish fodder. The terrestrial environment in the surroundingarea is mainly marshes and it is possible that allochthonous material in the formof humus supplies significant amounts of organic matter to the system.
This study forms a part of the project 'Eutrophication of Inland Waters' financedby The Royal Norwegian Council for Scientific and Industrial Research, and hasalso received support from BP-Norway Ltd.
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Received on November 4, 1987; accepted on May 11, 1988
