FEMS Microbiology Ecology 31 (1985) 215-223 215 Published by Elsewer

FEC 00027

The relation between bacterial carbon and dissolved humic compounds in oligotrophic lakes

(Limnetic bacteria; humic carbon supply; phytoplankton biomass; zooplankton grazing; multiple regression)

Dag O. Hessen

Dtt,tslon of Zoologr.. Department of Btologv. Umversl(v of Oslo, P 0 Box 1050. Bhndern, N-0316 Oslo 3. Norway

Received 22 March 1985 Revision recewed 14 May 1985

Accepted 28 May 1985

1. SUMMARY

The mean annual biomass of planktonic bacteria showed large variations both within and between lakes. The lowest bacterial biomass was found in acidified lakes (7.8-12.1 ~g C. l - l ) , and tended to increase with increasing water colour (up to 44.1 ~g C. 1-~). The highest recorded bacterial biomass was 138 /~g C-1-1. The mean annual bacterial biomass equalled 23-45% of the algal biomass. Zooplankton biomass was high, compared to algal biomass (40-50%). Multiple regression analysis of 10 variables showed a strong positive correlation between bacterial biomass and humic content ( r = 0.74, P < 0.001), while other parameters, except pH, showed no correlation. The observation thus strongly supports the role of humic compounds in aquatic secondary production.

2. INTRODUCTION

Although the presence of large numbers of pelagic bacteria in most aquatic environments has been known for decades [1-3], the role of aquatic

bacteria has been accorded serious interest only during the last 10 years. To date, bacterial biomass and production have been examined in eutrophic, [4-7] mesotrophic, [8] and oligotrophic lakes [9,10]. Humic lakes, or brown-water lakes, constitute a large proportion of the lakes in the holarctic re- gion, and most lakes in this area are more or less influenced by humic substances. The biomass and function of pelagic bacteria in humic and acidified lakes has been little investigated, although these organisms are probably of great importance to the overall metabolism of such lakes, owing to the high ratio of particulate organic carbon (POC) and bacterial carbon (BC) to algal carbon (AC) [10-12]. Both bacterial and zooplankton biomass are high compared to phytoplankton biomass and produc- tion, further indicating that allochthonous material is essential in the carbon pool [10].

6 Lakes of different humic content, with differ- ing fish and zooplankton communities and differ- ent chemical composition, were followed to reveal the annual changes in bacterial biomass. 2 Acidified, slightly humic lakes were also studied for comparison. Correlation between humic con- tent and bacterial biomass was examined in 6 brown-water ponds in summer.

0168-6496/85/$03.30 © 1985 Federation of European Microbiological Societies

216

3. MATERIALS A N D M E T H O D S

Monthly samples of bacterioplankton were taken during 1983 m all 8 lakes. With the excep- tion of one shallow, unstratified lake (H1), both epi- and hypolimnetic samples were taken. At regular intervals, replicate samples were taken, to test the validity of the results obtained from single samples (duplicates in March and September, tri- plicates in May and July). The replicates showed high conformity, and the SD was normally too small to be included in the figures. The main characteristics of the locations are shown in Table 1. Mid-summer samples were taken from 6 neighbouring ponds situated close to lakes H1 and H2. Bacteria were fixed in 2% formalin (final concentration) in 50-ml, brown glass bottles and stored in a refrigerator prior to staining with acridine orange and counting with an epifluores- cence microscope [13]. Even distribution of bacteria on filters was obtained by pre-wetting the filters with 1% Deconex solution. Bacteria from 6 differ- ent fields, or at least 200 cells, were counted on each filter. Volumes were calculated from 50 cells/filter by use of a micrometer ocular, calibrat- ed with monodisperse, fluorescent latex spheres with defined diameters. For conversion to carbon, the factor 1.21 × 10 -13 g C-/.tm -3 was used [14]. The term biomass, expressed as carbon, will, according to this method, also include dead and inactive bacteria.

Zooplankton was collected from all localities with a Ruttner sampler (4 1 from each depth), preserved with acid Lugol and counted and mea- sured (total length) with a Leitz binocular micro- scope. Dry weights were estimated from length according to Bottrell et al. [15] and Larsson [16]. A dry-weight-to-carbon conversion factor of 0.4 was used [17].

Phytoplankton was investigated in 3 selected humic lakes with different levels of humic con- tents. Counting was performed with an inverted microscope, according to the Utermohl technique [18]. Biomass (wet wt.) was calculated from geo- metrical models, and 10% of phytoplankton wet weight was calculated as carbon [19]. Data on chemistry, phyto- and zooplankton from the acidified lakes are derived from the Norwegian Liming ProJect.

Measurements of pH were made with a Metrohm 632 pH meter immediately after sam- pling, conductivity with a WTW LF 91 conductiv- ity meter, and 02 concentration by the Winkler method. Winter, spring, summer and autumn val- ues for Ca, Mn and Fe were obtained with an Atomic absorption spectrophotometer, (Perkin Elmer 603) and organic matter, expressed as mg 02 • 1 ~ was measured by KMnO:t i t ra t ion . Humic contents were measured as absorbance at 254 nm after centrifugation, using an LKB 8300 Uvicord 2 detector.

To reveal the relative importance of the various

Table 1

Characteristics of the Iocalittes investigated

Mean values are shown for KMnO4-oxldatlon and Ca, which showed little annual variation.

Lake Symbol Position Altitude Area Z.,.,~ Absorbance Secchi KMnO 4 pH K25 Ca (m) (m 2) (m) 254nm (m) (O2/1) (#S-cm -1) (p.g.1 - I )

Velttjern H1 61° l l 'N-10°31 'E 686 15000 3 0.120-0.174 3.0 5.24 5.60-6.64 13-27 1.62 Abbortjern H2 61o07'N-10°30'E 486 80000 15 0.032-0.129 5.2-7.1 6.84 6.61-7.35 20-35 5.51 Vesletjern H3 61°I3 'N-10°15'E 190 25000 7 0.188-0.242 2.9-4.3 6.63 5.62-6.40 22-39 1.24 Stensrudtjern H4 59°49'N-10°53'E 133 27000 8 0.149-0.190 2.5-3.5 10.01 6.40-7.90 80-170 9.37 Setertjern H5 59°58'N-10°48'E 286 8000 7 0.228-0.306 2.2-3.0 10.29 6.10-7.20 75-200 9.23 Flaskebekktjern H6 59°50'N-10°40'E 92 76000 9 0.426-0.680 1.0-1 2 9.77 5.41-6.14 56-80 2.99

Lille FinnetJern A1 58°56'N-8°51'E 237 7000 6 0.110-0.139 d 2.0-4.0 4.58-5.30 15-29 1.5 Kjelllngtjern A2 58°56'N-8°52'E 226 28000 12 0.100-0.110 a 3.0-5.5 5.02-6.24 10-25 1.2

d Estimated from Pt-values

biological and physico-chemical parameters on bacterial biomass, a stepwise multiple regression analysis was performed, testing the influence of humic concentration (absorbance), oxidisable or- ganic matter, temperature, O2-concentration, con- ductivity, Ca 2+, pH, biomass of cladocerans and rotifers and algal biomass as independent varia- bles. Only epilimnetic data were used, as the hypo- limnetic values would be strongly influenced by oxygen depletion, sulfide and iron concentrations, etc., affecting the large chemoheterotrophs.

4. RESULTS

Bacterial biomass showed great variation with seasonal, depth and inter-lake patterns (Figs. 1 and 2). The lowest annual biomass was recorded in

217

acidified lakes, with 7.8 and 12.1 /~g C-1-1, r e -

s p e c t i v e l y , and the large, slightly coloured lake H2, with an annual mean of 10.5 #g C • 1 -] . The other localities ranged from 16.2 (HS) to 44.1 (H6) #g C- 1-1 (means of epi- and hypolimnetic values).

Coinciding with autumnal oxygen depletion in the hypolimnion of lakes H3, H4, H5 and H6, there was a strong increase in bacterial biomass, reaching more than 100 #g C. 1-1 in lakes H4, H5 and H6 (138 #g C-1-~ in H6). During this condi- tion there was a dominance of large rods, in contrast to the dominance of small cocci in most of the samples.

Mean cell numbers ranged from 0.64 and 0.87 × 10 6. m1-1 (lakes A2 and A1, respectively), to 3.13 × 10 6. m1-1 (H6) (Table 2). The highest re- corded number was 5.44 × 10 6 (H6). As a rule, higher mean cell numbers were found in the hypo-

p g C . I "1

100-

50'

H1

i ! i ! ! ! i ~ O ! i i I i i I i

H / , :

.................. t t 1 0 0 " ~ ; ~ • I t •

o t

l I " / I I t i I

so- - " / •

J 'F'M=A~M= J ~j IA=S~OWN~l

H2

i v i w I i w i i i i

H5

I t r ;

a t A

./ i

J ' F ' M ~ A ' M ' J ' j wA'S~O'N' D

H 3 "

. . . . . . . . ; ' i ' i ' ' H6 ; ' ,

r j i

• . i t . . . .

l I • I t A

j ~ F ~ M ~ A W M ' j ' j ' A ' ~ O ' N ' D

Fig. 1. Bacterial biomass (#g C.1 - I ) in epilimnion (o) and hypolimnion (O) in the humic lakes H1-H6. Oxygen epilimnion (ml 0 2 • 1 - i ) indicated as triangles. Periods of ice-cover are shown as stippled bars.

mlOz.I -I (hypolimn.)

6

5

3

2

1

content in

218

/ugC'I-1 A1

50 - ,.:.:.:.::.:.:.:.:-:: " -:::">

4 0 -

30- /'~ t ~ 0~0

20 - " /

10-

1 I J I I ! I i I I

A2

50 - :.: .:-::-:::.:.::.::. . :-: -~

4 0 -

3 0 "

I0 . . . . ,

j I F I M I A I M I j I j IA IS lOWNJO

Fig. 2. Bacter, al biomass (fig C.1 1) m epl- and hypohmmon tn acidified lakes A1-A2. Symbols as in Ftg. 1.

limnion, owing to the autumnal peak already men- tioned. Mean cell volumes were almost equal in the epi- and hypolimnia of all lakes, within the range of 0.076-0.144 ~m 3. cell -1 (Table 2). The

largest cells were found in the hypolimnion of lake H3, where mean cell sizes > 0.2 #m 3 were fre- quently recorded. Although these mean values (Table 2) do not reflect seasonal changes, they should indicate the mean yearly differences wlthm (as SD) and between the various locations. The number of attached bacteria never exceeded 10% in any lake.

The regression matrix showed no correlation between bacterial biomass and physico-chemical parameters (except pH), oxidisable carbon, algae or zooplankton. Humic contents (UV-absorbance) were, however, strongly correlated to bacterial bio- mass ( r = 0.74, P < 0.001), while pH was nega- tively correlated ( r = -0 .50, P < 0.02). Thus, the equation relating bacterial biomass (V B) and UV and pH is

V B = 0.795 × UV2s 4 - 0.0908 x pH + 0.630.

Together, UV and pH explained 66% (r 2) of the observed changes m biomass. Partial regres- sion coefficients from both parameters gave a sig- nificant contribution to the regression. If UV and pH are taken as independent variables (they were not significantly correlated), pH could explain 11% of the total variance in bacterial biomass (calcu- lated by stepwise regression). In the 6 ponds, which did not differ with respect to climatic or hydrological conditions, numbers of bacteria were also positively correlated with UV (r = 0.71, P < 0.001) and negatively correlated with high pH ( r = - 0 . 6 6 , P < 0 . 0 5 ) (including lakes H1 and H2) (Table 3).

4.1. Phytoplankton Within the 3 humic lakes H3, H5 and H6, by

far the highest biomass was found in lake H5, with

Table 2

Mean bacterial numbers and cell volumes in epihmn,on (E) and hypolimmon (H)

SD m parentheses

Lake H1 H2 H3 H4 H5 H6 A1 A2

Mean no. E 2.27(0.42) 1.21(0.59) 1.87(1.21) 1.88(0.78) 1.10(0.56) 3.13(1 54) 0.87(0.36) 0.64(0.27) (106. ml - ] ) H 1.23(0.51 ) 1.91(1.33) 2.22(1.36) 2.62(1.77) 2.98(1.26) 0.99(0.45) 0.86(0.28)

Mean cell E 0.092(0.020) 0.090(0.021) 0.124(0.032) 0.099(0.029) 0.144(0.045) 0.126(0.042) 0.121(0.042) 0.111(0.032) v o l u m e ( f m 3) H 0.076(0.012) 0.121(0.038) 0.090(0.032) 0.142(0.052) 0.124(0.061) 0.176(0.044) 0.103(0.017)

~KjC.I - ̧

200 ¸

100

200

100

200

100-

H5 E

H3 E

H6 ' ~

r A I M I J = j = A I S r O ~ N ~ I

i 1 H

D---o 7..Ool~ankton H H Phytoldankton

c~ - .o Bacterioplankton

,' ',

J IF J I A I S l O I N I

Fig. 3. Biomass (/xg C . l - t ) of zooplankton , phy top l ank ton

and bac te r iop lank ton in ep i l immon (E) and hypo l imnion (H) m

lakes H5, H3 and H6.

a maximum in October of almost 300 #g algal C. 1-l (Fig. 3), contrary to a maximum in spring (April) of only 110 #g C. 1-1 in lake H3. These two shallow lakes had similar biomass and algal composition in both epi- and hypolimnion, whereas the deeper and more strongly coloured lake H6 showed a strong decrease of algae in the hypolimn- ion. All these localities exhibited high numbers of Cryptomonads and Peridinium spp. The frequency of different size classes of algae are shown in Table 4. In certain periods, the phytoplankton community was dominated by very large species ( > 40 #m), especially in lakes H5 and H6.

Phytoplankton biomass in acidified lakes was dominated by Cryptophyceae and Chrysomonads.

219

Tab le 3

Abso rbance (254 nm), pH, total number and cell vo lume m June and July from 6 ne ighbour ing ponds and local i t ies HI and

H2.

(Absorbance measured only in June).

Pond ,4254 pH N )< 106 Volume (/~m 3)

1 0.180 6.80-6.95 0 .67-0 .89 0,078-0.083

2 0.297 6.35-6.42 1.29-1.33 0 .073-0.090

3 0.315 4 .77-4 .90 2.10-2.77 0.060-0.075

4 0.344 4.78-5.13 2 .04-2.46 0.120-0.148

5 0.561 5 18-5 .60 2 .16-2.60 0.090-0.112

6 0.652 4 .63-4 .94 2.37-2.51 0.070-0.093

H1 0,125 5.95-6.36 1.56-1.94 0.086-0.105 H2 0.215 6.65-6,95 0 .81-1 .54 0 .092-0,100

While lake A2 had a low annual b iomass (mean annual: 31 ~ g C • 1-1, m a x i m u m in late June of 90 ~ g C - l - t ) , lake A1 exhibited high phytoplankton b iomass (mean annual: 156 # g C • 1-1, m a x i m u m in June or more than 5 0 0 / t g C • l - l ) .

4.2. Zooplankton Although zooplankton composition showed a

great deal of annual and interlake variation, the mean yearly zooplankton biomass is strikingly similar in the humic lakes (approx. 60 #g C- 1- .) with the exception of the strongly coioured lake H6 (Table 5). This lake also differs strongly in zooplankton composition, as the entire yearly bio-

Table 4

Size-groups of a lgae (bt m), epi l imnion.

Expressed as % of total blomass.

Local i ty S ize /p .m M J J A S O

H3 < 5 - 33 18 91 43 5 - 2 0 37 - 46 6

2 0 - 4 0 63 67 1 3 57

> 40 - - 28 - -

H5 < 5 4 2 8 1 18 5 - 2 0 65 35 7 23 31

2 0 - 4 0 6 5 4 - 27

> 40 27 57 81 76 24

H6 < 5 - - - 8 14

5 - 2 0 25 4 59 12 16

2 0 - 4 0 75 - - 54 70

> 40 - 96 41 26 -

22O

Table 5

Relat,ve ,mportance of zooplankton groups

V = ~g C. 1 1. Mean for epi- and hypolimnion (C = 40% of dry wt.)

HI H2 H3 H4

V % V % V % V %

H5 H6 AI * A2 *

V % V 9~ % %

Rotifera 0.8 1 0 8 1 0.2 1 19 8 Copepoda 24.7 39 28.6 46 30.7 48 27.0

Cladocera 38.1 60 32.6 53 33.2 52 21.0

Zooplankton 63 6 62.0 64.1 67.8

29 17.4 25 0.9 2 35 60 40 17.2 25 0.4 1 50 35

31 34.9 50 45 3 97 15 5

69.5 46.6

* Esumated from verttcal net hauls.

mass is made up by a mid-summer peak of the cladoceran Holopedium gibberum. Lakes H4 and H5 also differ from the others with respect to high conductivity and large stocks of planktivore fish. For this reason, the crustacean zooplankton is dominated by small bacterivores, such as rotifers and the cladocerans Bosmina longispma, Bosmina longtrostris and Ceriodaphnia quadrangula. The shallow lake HI is also heavily stocked with small perch, and has almost a monoculture of the cladoceran B. longispina, while H2 and H3 are dominated by the cladocerans H. gtbberum, Daphnia longispma, B. longlspina and C. quadran- gula. Small numbers of Diaphanosoma brachyurum and the calanoid Eudiaptomus gracdis were found in all localities.

Lakes A1 and A2 were both dominated by rotifers. Lake A2 was almost completely dominated by rotifers, while in lake A1, the zooplankton community was dominated by rotifers in winter, and cyclopoid copepods in summer. Cladocera were sparse, except in July when D. brachyurum occurred in high numbers (30 organisms • 1-1).

Ciliates and heterotrophic flagellates were counted in the phytoplankton samples, but found only in inferior numfers . The highest recorded biomass of these organisms was 3 #g C . 1-1 in lake H5 (March).

5. DISCUSSION

A mean annual biomass in the range of 7.8-12.1 /~g C • 1 - t (acidified lakes), 10.5 #g C- 1 - t (slightly

coloured) and 16.2-44.1 /~g C. 1 i (humic lakes), falls within the range of earlier observations, e.g., 6 -14 ~g C . 1 - i in an oligotrophic lake [9], 20-100 in humic lakes [10,12] and 80-130 ~g C . 1-1 in eutrophic lakes [5-7]. Andersson [20], however, found a surprisingly high biomass in the acidified Lake G~rdsji3n, of almost 50 ~tg C . 1-1

Mean cell number increased with increasing mean cell volume in all localities, possibly' owing to increased frequency of dividing cells (FDC) and thus larger bacteria during population growth as bacterial volumes tend to increase prior to division [21]. The largest cell numbers and cell volumes were found in the 2 most humic localities. Cell volumes in the range of 0.07-0.23 ~m 3 agree with most of the data in the literature, e.g., oligotrophic lakes: 0.04-0.24 /~m 3 [22]; 1 # m 3 [9]; 0.06-0.16 #m 3 (Hessen, unpublished). Humic lakes: 0.09- 0.25 #m 3 [10]; 0.17-0.32 ~m 3 [12]; 0.03-0.24/.tm 3 (mean 0.132) [23]. Eutrophic lakes: 0.10-0.16/zm 3 [5]; approx. 0.16 # m 3 [6]. For acidic lakes, Traaen [24] reported a mean cell volume of < 1 t.tm 3, Hessen [25] found 0.05-0.18 #m 3 while an ex- tremely high mean volume was found by Anders- son [20], with 0.34 btm 3.

Bacteria constituted a large fraction of the planktonic biomass in the lakes tested. As annual mean, bacteria equalled 23-45% of algal biomass, and in certain periods even exceeded both phyto- and zooplankton biomass.

Relatively high numbers of bacteria in humic lakes compared to those in oligotrophic clearwater lakes have previously been reported [2,26,27,12]. In most clearwater lakes, both oligotrophic and

eutrophic, bacterioplankton is equivalent to 10- 30% of phytoplankton biomass [5-7,9]. A similar ratio exists between bacterial production and primary production. Clearwater lakes with a high input of allochthonous material may exhibit a larger proportion of bacteria, e.g., 35-40% (bio- mass) in oligotrophic 0vre Heimdalsvann [28] and near 70% (production) in eutrophic Lake Plussee [29], as compared to phytoplankton biomass and production, respectively.

In humic lakes, secondary bacterial production has been found to be equivalent to more than 70% of primary production [10,11]. In some lakes, bacterial biomass and production even exceed those of the algae [12].

Several biotic factors may influence community structure and cell sizes of bacteria, among which zooplankton grazing is probable, but difficult to assess. Of the zooplankton present, both rotifers and most cladocerans are potential consumers of bacteria. While Holopedium sp. is regarded as a poor filterer of bacteria, Daphnia spp., Bosmina spp., Ceriodaphnia quadrangula and Di- aphanosoma brachyurum have been shown to be efficient consumers of bacteria [30-32]. Although no correlation was found between zooplankton and bacterial biomass, there is in most lakes a drop in mean bacterial cell size coinciding with the peak in cladocerans, and an autumnal increase after the decline of cladocerans. Whether this is due to removal of the largest bacteria by grazing, or just to a change in growth conditions, is impos- sible to say. Pedrbs-Alib and Brock [6] found zooplankton grazing to be of minor importance to standing microbial biomass in a eutrophic lake, but did not discuss its importance to mean bacterial volumes. On the other hand, the presence of a high bacterial biomass is likely to have a positive in- fluence on zooplankton biomass and production, indicated by the high zooplankton : phytoplankton ratio.

Salonen and Hammer [33], suggested that detri- tus and bacteria are the main food sources for filtering zooplankton in such lakes. Although phy- toplankton biomass exceeded bacterial biomass in all localities, the phytoplankton community often comprised a major fraction of large ( > 40-50 ttm) algae (Table 4). Most of these would not be availa-

221

ble as food to most species of zooplankton [34,35], thus further stressing the importance of bacteria to the 'micro-filterers', in humic lakes. Although only 5-10% of the bacteria were attached, larger par- ticles were always crowded with large rods, thus providing a food source even for the non-filtering copepods.

A positive relationship between algae and bacterial biomass is well known from clearwater lakes [6,8,36]. In the 2 acidified lakes, bacterial biomass seemed mainly dependent upon algal bio- mass. In the humic lakes, however, bacterial bio- mass often shows a peak before an algal bloom (Fig. 3), in contrast to what is usually found in clearwater lakes.

The present results suggest that the influence of humic compounds is of major importance to bacterial biomass throughout the year. Although factors like primary production, chemical proper- ties, climatic conditions, zooplankton grazing etc. probably influence the composition of the bacterial communities in these lakes, the only significant contributor to bacterial biomass was humic con- tent.

Maximum biomass in all lakes coincided with peaks in absorbance, due to the main periods of run-off in spring and autumn, which provides a source of humic compounds to the lakes, as well as an inocolum of soil bacteria. The underlying mechanisms for the bacterial utilisation of these refractile substances are as yet unknown. The humic compounds themselves [37,38], as well as chelated or bound ions [39], may be the source of nourishment.

The apparent influence of low pH is striking. Although this could be partly explained by the positive correlation between humic compounds and pH, this correlation was insignificant. Although the acidity produced by bacterial metabolism is probably minimal compared to the acidity gener- ated by humic input, it might support the lowered pH in these lakes. In any case, this suggests that the low number of bacteria in acidic lakes might be due to low humic content or low primary production as well as to low pH in itself. Even strongly acidic lakes may exhibit large numbers of bacteria when coloured [12,14].

222

A C K N O W L E D G E M E N T

I am most grateful to Eirik Fjeld for help and comments on statistical analyses, to Dag Klave- ness and John G. Ormerod for valuable comments on this manuscript and to my colleagues in the Norwegian Liming Project. The study was partly supported by The Norwegian Council for Human and Natural Sciences (NAVF).

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