Variation in growth rates of submerged rooted macrophytes

Aquatic Botany, 39 (1991) 109-120

109

Elsevier Science Publishers B.V., Amsterdam

Variation in growth rates of submerged rooted macrophytes Soren Laurentius Nielsen and Kaj Sand-Jensen Freshwater Biological Laboratory, University of Copenhagen, 51 Helsingorsgade, DK-3400 Hillerod (Denmark) (Accepted for publication 11 June 1990)

ABSTRACT Nielsen, S.L. and Sand-Jensen, K., 1991. Variation in growth rates of submerged rooted macrophytes. Aquat. Bot., 39: 109-120. Above-ground growth rates of 14 temperate, submerged freshwater macrophytes were measured in the laboratory at high dissolved inorganic carbon levels (3.3-3.8 mM), nutrient saturation and photon flux densities (photosynthetically active radiation (PAR) ) of 14.4 mol m - z day - t at 15 ° C. Growth rates ranged from 0.007 to 0.109 day- ~, corresponding to doubling times of 95 and 6.4 days. Growth rates of selected species measured at low shoot densities in the field during summer resembled the laboratory rates. The carbon affinity during photosynthesis accounted for 61% of the observed variability in growth rates. These results support previous findings demonstrating the importance of carbon utilization for the distribution, abundance and growth of submerged macrophytes. The carbon affinity was a constant attribute for some species, including the slowly growing rosette species, but changed during acclimatization in the laboratory for other species. Morphological features (e.g. the surface/volume ratio ) were unable to account for much of the variability in growth rates.

INTRODUCTION

Submerged macrophytes play a major role in the dynamics of shallow lakes and small low-gradient streams. They are often the main primary producers in these shallow freshwater habitats (Wetzel, 1983; Kelly et al., 1983 ). Their abundance influences the biomass and productivity of other primary producers (Carpenter and Lodge, 1986; Sand-Jensen et al., 1988). Their surfaces provide a substrate for epiphytic algae and bacteria, and for grazing and filtering invertebrates (Iversen et al., 1984). Macrophyte populations stabilize the sediment against erosion and promote sedimentation of mineral and organic particles (Ward et al., 1984; Sand-Jensen et al., 1989). Consequently, there is growing interest in the factors that control macrophyte development and their impact on freshwater ecosystems. 0304-3770/91/$03.50

© 1991 I

Elsevier Science Publishers B.V.

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Recent investigations have emphasized the importance of light, sediment nutrition, and the morphometry and hydrology of lakes and rivers for the abundance of submerged macrophytes (Carignan and Kalff, 1980; Barko and Smart, 1981; Chambers and Kalff, 1985; Duarte and Kalff, 1986; Sand-Jensen et al., 1989). Several investigations have also shown the major role of light in the growth rate of single species under in situ conditions (Kemp et al., 1987; Sand-Jensen et al., 1989). However, there are no investigations of the differences in growth capacity among submerged macrophyte species. Consequently, we set out to compare the growth rates of several submerged rooted macrophytes under attempted optimum conditions in the laboratory and, if possible, to predict the growth rate from morphological and physiological features. The growth rate will ultimately determine the ability of the species to recover and develop dense stands following pronounced reduction of abundance during unfavourable periods, and during mechanical harvesting or herbicide treatments. Moreover, the growth rate will influence the ability to outcompete other species under crowded conditions. To ensure a wide range of growth rates, we selected species known from previous investigations to grow slowly versus rapidly under field conditions, comprising slowly growing rosette species with high CO2 compensation points and no ability to utilize HCO~- (Sand-Jensen and Sondergaard, 1978; Sand-Jensen, 1987 ), as well as rapidly growing species with the ability to utilize HCO~- and to develop dense canopies. We hypothesize that carbon affinity and plant morphology are probably important determinants of growth rates. As a measure of plant morphology, we used the relative surface area of the assimilating shoots which is a good predictor of maximum growth rates for phytoplankton species (Reynolds, 1984). Finally, the chlorophyll concentrations in the assimilating shoots were used as a measure of the light-harvesting capacity of the plants. For single plant species, many investigations have shown a relationship between light absorbence, photosynthesis and chlorophyll concentrations in the tissues (e.g. Raven, 1984). METHODS

Growth conditions Fourteen rooted macrophyte species submerged in Danish streams and lakes were collected during October 1987. The plants were grown submerged in large aquaria in the laboratory. Single shoots were planted in plastic pots (diameter 7 cm, depth 15 cm ) in a sandy sediment from the hardwater Esrom stream. Depending on the growth form, apical shoots or new lateral shoots were replanted at intervals and allowed to root to maintain small plants in rapid growth. Lobelia dortmanna L. and Littorella uniflora (L.) Aschers. grow

GROWTH RATES OF SUBMERGED ROOTED MACROPHYTES

111

slowly and continuously replace the leaves on the short stem, and did not need replanting. To ensure sufficient nutrient supply, a commercially available slow-release fertilizer normally used for potted plants was added at regular intervals. The plants were set at low density in 50-cm deep thermostated perspex aquaria (volume 5001 ). The aquaria were illuminated by fluorescent light tubes from above at a photon flux density of 250/tmol m -2 s- 1 (photosynthetically active radiation (PAR)) and kept in a 16-h light/8-h dark cycle at a temperature of 15 ° C. The aquaria contained an equal mixture of tap and distilled water with a high alkalinity (3.7 meq 1-1, resembling the conditions under which the plants were growing in the field) and a high concentration of dissolved inorganic carbon at 3.3-3.8 mM dissolved inorganic carbon (DIC) (measured by Gran-titration; Stumm and Morgan, 1970). We added a commercially available solution of micronutrients normally used for aquarium plants to maintain sufficient concentrations of micronutrients in the water. One-third of the water was replenished every week and filamentous algae were removed when necessary by gently wiping the plant surfaces with soft tissue. The water was constantly aerated with atmospheric air and circulated by a submersible Eheim pump to avoid appreciable 02 and pH build-up during photosynthesis, and to avoid thick boundary layers surrounding the plant surfaces. The pH was kept at 8.2-8.6 during the light period so the CO2 concentrations in the water ( 14-50 aM CO2, calculated from Rebsdorf, 1972 ) were close to equilibrium with CO2 concentrations in the atmosphere. Growth rates

After acclimatization for at least 4 weeks, 10 small individually potted plants of every species were transferred to a new aquarium and grown at low density to avoid shading among neighbours. Growth conditions were the same as those described above. The plants always looked green and healthy. The growth rate of above-ground parts was determined by measuring shoot length, shoot number, and the length and width of leaves for every plant at 3-7-day intervals during 4-6 weeks. For plants without an erect stem, we only measured the number and dimensions of leaves. Moreover, we followed leaves and side-branches that became senescent and were lost. After 4-6 weeks, the plants were harvested and roots, stems and leaves of every plant were freezedried and weighed. The cumulated above-ground biomass of each plant (including losses) at every measurement was calculated using corresponding values for dry weight and length-width of leaves, and length of stems. These corresponding values were only determined at the end of the experiments. However, determinations of the same relationships for small shoots of the same size as those planted at the onset of the growth experiment revealed no significant differences over the size and age ranges used here. The plants grew exponentially with time and the growth rate (ln units day- 1) was calculated

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S.L. NIELSEN AND K. SAND-JENSEN

as the slope of the linear regression of In cumulated biomass with time. As the plants were planted in natural sediment, no determination of root growth rate was possible. All growth rates thus represent above-ground growth rates.

Carbon affinity and photosynthetic rate The carbon affinity and photosynthetic rate of leaves of all species were measured at the termination of growth experiments using the same type of water as during growth. The carbon affinity was also measured immediately for some of the collected species prior to laboratory incubations of the plants. All experiments were carried out in closed glass bottles mounted on a rotating wheel in a thermostated incubator ( 15 °C) at a photon flux of 390/~mol m - 2 s- 1. The experimental water was bubbled with atmospheric air before the experiment to bring it to equilibrium with 02 and CO2 in the air. Carbon affinity was measured in drift experiments where the pH was allowed to increase from 8.0 to its m a x i m u m achievable value over at least 24 h of continuous illumination. This "end p H " reflects the ability of leaves to extract CO2 and HCO~- from solution since CO2 is rapidly depleted as pH increases. The photosynthetic rate was measured as 02 evolution in short-term experiments by determining the initial and final 02 concentrations by Winkler titration (Golterman, 1969 ). This method underestimates the true rates of photosynthesis by only 2-3% (based upon the measured gas volumes of the incubated plants) when 02 in the lacunae and the surrounding water is assumed to be in equilibrium.

Morphometric features The relative leaf biomass of plants was calculated as the proportion of leaves of the total biomass of freeze-dried samples after the growth experiments. The relative surface area was calculated both as m 2 g- ~ dry weight (DW) and m 2 m-3. The rationale for determining both ratios was that submerged macrophytes may possess an extensive lacunal air system so that thick tissue with a low m 2 m -3 ratio may have a proportionally higher m 2 g-1 DW ratio. On the other hand, the lacunal air system may also facilitate internal gas transport and refixation of respired CO2 (Sondergaard, 1979 ). The above-ground parts of four plants of every species were analysed for surface area by a LiCor area meter (Li 3000), for dry weight by freeze-drying and for volume by a pycnometer. To calculate the entire surface areas of plants, we multiplied the projected surface area (measured by the area meter) by two for plants with flat leaves, by z~for plants with cylindrical leaves and by three for Sparganium erectum L. with triangular submerged leaves. The dimensions of the leaf filaments of Myriophyllum spicatum L. were too small to be registered reliably

GROWTH RATES OF SUBMERGED ROOTED MACROPHYTES

I 13

by the area meter. Instead, we measured the dimensions of the cylindrical leaf filaments with a microscope.

Chlorophyll concentration Above-ground parts of freeze-dried plants were added to a small amount of distilled water, ground in a mortar and extracted in 96% ethanol. The solution was filtered, and chlorophylls a and b were measured spectrophotometrically and calculated following Wintermans and DeMots ( 1965 ).

Statistics The variables were all determined with some variance. The relationship among variables was analysed by correlation analysis since all data sets, except the relative surface area, were normally distributed. The data sets for relative surface area were normalized by logarithmic transformation. RESULTS

The above-ground growth rates and morphological-physiological features of the 14 rooted macrophytes derived from the growth experiments are given in Table 1. Eight of the 14 species always grow submerged (s) and two of those develop floating leaves (s-f). The two rosette species usually grow submerged, but are occasionally emerged (s (a)). Four species are amphibious (a) and frequently grow submerged in streams. However, all 14 species were grown submerged in the present experiments. The growth rate ranged from 0.007 to 0.109 day-~, corresponding to doubling times for the above-ground biomass of between 95 and 6.4 days. The two rosette species, Lobelia dortmanna and Littorella uniflora showed the lowest growth rates (0.007-0.009 day - l ) . Growth rates were also lower (0.020-0.042 day -~ ) for three of the amphibious species, Berula erecta (Huds.) Coville, Myosotis palustris L. and Sparganium emersum Rehman, than for those species always growing submerged (0.046-0.097 day- ~). However, the amphibious species, Sparganium erectum, showed the highest growth rate of all species tested (0.109 d a y - ~). Carbon affinity was the only variable that was significantly positively correlated with growth rate ( r = 0.765, P < 0.01, Table 2 ). Photosynthetic rate and relative surface area were also positively related to growth rate, but the correlations were poor (Table 2 ). The chlorophyll concentration was significantly positively correlated with the relative leaf biomass and the relative surface area (Table 2 ), and the latter two variables were also significantly positively interrelated. The two indices for relative surface area were also significantly positively related.

s

Elodea canadensis

0.007 _+0.001

0.009_+0.001

0.020_+ 0.002

a=amphibious;s=submerged;f=floating-leaved. *From Sand-Jensen (1987). **From Sand-Jensen and Sondergaard (1979).

Lobelia dortmanna L.

Ascherson

s (a)

s(a)

Littorellauniflora (L.)

(Hudson) Coville

a

Berula erecta

0.030_+0.002

0.042_+0.003

a

a

0.046 _+0.004

0.052 _+0.005

s

s

0.067 _+0.008

s

Myosotispalustris L.

Rehman

Myriophyllum spicaturn L. Sparganiumemersum

L.

Potamogeton panormitanus Biv. Potamogeton crispus

L.C. Rich.

0.086 _+0.004

0.094_+ 0.005 0.088_+0.010

s s-f

Sendtner

0.094 _+0.008

s

0.097 + 0.006

0.109-+0.016

Above-ground growth rate (In units d a y - l )

Potamogeton pectinatus L. Potamogeton densus L. Callitrichecophocarpa

( L. ) Wimmer

Batrachium aquatile

s-f

a

Sparganiumerectum

L.

Habitat

Species

8.80_+0.02 (8.80_+0.01 8.91 _+0.01 (8.99_+0.07 8.95 -+ 0.01 ( 8.75 _+0.00 8.39+0.02 ( 8.10* ) 8.18 _+0.05 (8.10")

9.26 + 0.16 (9.97_+0.05 8.80 _+0.04

9.60_+0.30 (8.74_+0.07) 9.47 -+0.08 ( 10.53 + 0.03 ) 9.07 _+0.30 ( 10.19 _+0.05 ) 8.99 + 0.08 8.82_+0.01 (9.06_+ 0.06) 9.44-+ 0.13 (9.65 _+0.26) 9.28 _+0.31

Carbon affinity (end pH )

0.59_+0.30

4.55-+0.99

3.39_+0.16

4.08_+0.35

7.26_+0.79

9.11_+1.04

17.98_+0.43

5.23-+0.52

5.16+0.45

15.40-+2.77 17.94_+1.74

3.91_+0.31

4.92-+0.44

5.63-+0.26

Photosynthetic rate (Pn) (mgO2g-tDWh -1)

4.29+0.08

5.25-+0.21

12.61_+0.33

8.42+0.43

8.89_+0.16

11.15_+0.26

4.15_+0.28

4.10-+0.10

3.62_+0.08

2.75-+0.09 12.19_+0.53

2.49+0.13

4.58-+0.42

7.95_+0.46

Chlorophyll concentration (mgchla+bg-~DW)

43.20_+ 6.12

37.50**

64.34+ 4.15

60.37-+ 6.82

67.47_+ 5.31

69.95_+ 2.82

41.34+ 7.32

36.65-+ 4.63

64.23_+ 10.53

40.08_+ 2.39 51.87_+10.02

37.36-+27.14

47.90-+ 4.34

Relative leaf biomass (%)

0.40_+0.02

0.40-+0.04

1.58_+0.10

1.12-+0.02

2.48_+0.16

2.10_+0.08

0.96_+0.24

1.22_+0.10

0.82_+0.06

3.12_+0.28

0.70-+0.06

0.56-+0.02

0.54+0.04

(m2g-~DW)

1.38

27.42-+ 0.98

30.34-+ 1.10

54.94_+ 0.94

44.90-+ 1.50

50.66_+ 1.00

108.92_+ 5.82

40.88_+ 6.24

57.90-+ 1.22

44.34_+ 4.26

102.18_+ 15.20 52.46+ 4.20

35.96_+ 4.46

43.74_+ 5.68

21.42_+

( m 2 m -3)

Relative surface area

Above-ground growth rate, carbon affinity, photosynthetic rate, chlorophyll concentration, relative leafbiomass and relative surface area for the 14 macrophyte species ranked in order of decreasing growth rate. All values are given as the mean _+SD. The habitat indices are explained in Methods. Number of determinations: growth rate and relative surface area ( n = 10); carbon affinity ( n = 2 ) ; photosynthetic rate ( n = 5 ) ; chlorophyll concentration ( n = 3 ) ; relative leaf surface area ( n = 4 ) . The carbon affinity for some of the collected species measured prior to growth experiments in the laboratory is shown in parentheses

TABLE 1

Z

m Z

Z

F

rn Z > Z

P Z

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GROWTH RATES OF SUBMERGED ROOTED MACROPHYTES

TABLE 2 Correlation coefficients between the measured variables growth rate, carbon affinity, photosynthetic rate, chlorophyll concentration, relative leaf biomass and relative surface area (n = 14). Partial correlation coefficients between growth rate and the other variables are shown below the line. Units are as given in Table 1 Variable

Carbon Photosynthetic Chlorophyll Relative affinity rate concentration leaf biomass

Relative surface area (m2g-tDW)

( m / m 3)

Growth rate Carbon affinity Photosynthetic rate Chlorophyll concentration Relative leaf biomass Relative surface area (cmZmg - 1 D W )

0.765*

0.085 -0.044

Growth rate

0.784*

0.333 0.146

-0.255 -0.171

-0.179 0.049

0.035 0.010

0.110

-0.099

0.538*

0.416

0.695* 0.710"

0.200

0.604*

0.300 0.668*

0.130

-0.126

-0.357

0.344

0.096

*Significant at P < 0.05.

The correlation coefficient between growth rate and carbon affinity increased only slightly by partial correlation analysis, which excludes the influence of the other measured variables (r=0.784, Table 2). The correlation between growth rate and the other measured variables remained low after this procedure. DISCUSSION

The growth rate of macrophytes in these experiments was calculated as the increment of above-ground biomass corrected for losses of senescent leaves and lateral branches. The measured rates represented the net primary productivity over 24 h, assuming that the extracellular release of organic carbon (EOC) from the non-senescent parts was negligible. This assumption was probably sound since the EOC release is usually a small proportion of photosynthetic carbon fixation under suitable conditions for macrophyte growth (Wetzel and Manny, 1972; Sondergaard, 1981 ). The macrophyte species had widely different growth rates under the same nutrient-rich, hardwater conditions in the laboratory. Most species also grow under these conditions in the field. The two rosette species, Lobelia dortmanna and Littorella uniflora, are often dominant species in softwater, oligotrophic lakes. However, they may also occur in eutrophic, hardwater lakes

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S.L. NIELSENAND K. SAND-JENSEN

(Farmer and Spence, 1986) and their usual absence from these habitats is probably due to shading from phytoplankton, epiphytic algae and more vigorously growing rooted macrophytes, and not to adverse effects of the high supply of inorganic nutrients and inorganic carbon (Sand-Jensen and Sondergaard, 1981 ). Even though the laboratory growth rates may not be the maximum attainable for all species, the growth rates nevertheless resembled those found for some of the species in field experiments under suitable light and temperature conditions during summer in Danish habitats (Table 3). The growth rates of the two rosette species were somewhat higher under laboratory than under field conditions, suggesting no adverse effects of the laboratory growth conditions. The different growth rates under similar laboratory conditions must reflect the differences in growth form, morphology and physiology among the species. The correlation analysis showed that the growth rate was positively related to relative surface area (m 2 g- 1 DW ) and photosynthetic rate, but only the relationships to carbon affinity were significantly positive. The "end pH" reached during photosynthesis in closed bottles was used here as an index of the ability to extract inorganic carbon from the medium. End pH is often used specifically as an index of the HCO~- affinity (Hutchinson, 1975), but this interpretation was avoided here as species with different CO2 compensation points attain different "end pH" without using bicarbonate. A species with a low CO2 compensation point may also reach a similar high "end pH" without using HCO~- as a species using HCO~- with low efficiency. Finally, the rate of CO2 release during respiration in the light will also influence the "end pH".

TABLE3 Comparisons of optimum growth rates of selected macrophyte species in the laboratory (this work) with those in field experiments with natural populations or with single potted plants during summer, all kept at low shading intensity from neighbours Species

Laboratory growth rates (day- ~)

Field growth rates (day-~ )

Batrachium peltatum Potamogeton pectinatus Elodea canadensis Potamogeton crispus Sparganium emersum Littorella uniflora Lobelia dortmanna

0.097 0.094 0.086 0.052 0.042 0.009 0.007

0.092 0.091 0.084 0.070 0.034 0.006 0.004

( 1 ) Norgaard (1989). (2) K. Sand-Jensen and N. Thyssen (unpublished, 1984). ( 3 ) Madsen and Sand-Jensen ( 1987 ). (4) Sand-Jensen and Sondergaard ( 1978 ).

(I) (2) (3) (!) (2 ) (4) (4)

GROWTH RATES OF SUBMERGED ROOTED MACROPHYTES

1 17

The carbon affinity may, therefore, provide an integrated picture of the carbon balance of the species in the light, taking both the carbon uptake and release into account, and show a closer relationship to the growth rate than the photosynthetic rate alone. Many previous investigations have stressed the importance of the supply and utilization of inorganic carbon as important factors for the adaptation, distribution, abundance and growth rates of submerged macrophytes (reviewed by Raven, 1970; Hutchinson, 1975; Spence and Maberly, 1985; SandJensen, 1987). The surfaces of rooted macrophytes are often surrounded by thick boundary layers which induce a high resistance to the utilization of inorganic carbon because the molecular diffusion of free CO2 is so much slower ( 104 times ) in water than in air. Many morphological and physiological attributes of submerged rooted macrophytes have therefore been explained as adaptations to increase the carbon gain of the plant, even though they may serve other functions as well (Sand-Jensen, 1987 ). These adaptive features include the thin and often finely dissected leaves, active utilization of HCO~-, dark fixation of inorganic carbon and exploitation of the alternative CO2 pools in the atmosphere and rhizosphere (Sand-Jensen, 1987). The carbon affinity of several of the laboratory-grown species conformed with previous experiments with plants collected in the field, but others did not. Lobelia dortmanna and Linorella uniflora from the field have high CO2 compensation points for photosynthesis and no apparent ability to use HCO~- (Sand-Jensen, 1987 ). These species also showed the lowest "end pH" values (8.18-8.39, Table 1). Sparganiurn emersum and Callitriche cophocarpa Sendtner from the field have no apparent affinity for HCO~-, but lower CO2 compensation points than the rosette species (Sand-Jensen, 1987) and showed intermediate "end pH" values (8.80-8.82), resembling those measured when the plants were collected in the field (8.80-9.06). Potamogeton crispus L. and Potamogeton pectinatus L., on the other hand, may have a high carbon affinity and drove pH to high values (9.97-10.19) directly after collection in the field. Other researchers, though, have found much higher "end pH" values for species like P. crispus, Potamogeton panormitanus Biv., Myriophyllum spicatum and Elodea canadensis L.C. Rich. than found in this investigation (Maberly and Spence, 1983). It has been shown, however, that the carbon extraction capacity in general, and the HCOy affinity in particular, is not a constant attribute of the species, but is under environmental control (Sand-Jensen and Gordon, 1986). Thus, the lowering of the carbon extraction capacity during growth under controlled conditions is probably due to the high carbon availability under the growth conditions used. Sand-Jensen ( 1987 ) has hypothesized that homophyllous amphibious species will be unable to utilize HCO; when growing submerged because the surface of the leaves is unsuitable for active transport processes. By inference, this should also lead to a limited capacity to extract inorganic carbon and to grow, except under CO2-rich conditions. The two homophyllous amphibious

118

S.L. NIELSENAND K. SAND-JENSEN

species (Berula erecta and Myosotis palustris) maintained the same relatively low "end pH" during the growth experiments (8.75-8.99 before and 8.918.95 after, Table 1 ) and grew relatively slowly (0.020-0.030 day-l, Table 1 ). Sparganium erectum, however, increased the carbon affinity during the experiments from 8.74 to 9.60 and showed the highest recorded growth rates (0.109 day-t, Table 1). The submerged leaves of Sparganium erectum are distinctly different from the emergent leaves and it is possible that the submerged leaves differ anatomically and physiologically from those of the homophyllous amphibious species. However, the submerged leaves of Sparganium emersum are also different from the emergent leaves, but this species maintained the same low "end pH" during the growth experiment (8.80) and showed an intermediate growth rate (0.042 day -1 ). Carbon utilization of amphibious plants is currently under investigation. CONCLUSIONS

The regulation of growth rates among rooted macrophytes is probably complex, depending on the growth form, other morphological features and physiology of the species. We regard the carbon affinity as the best, but not a fully satisfactory predictor of the different growth rates among species, even though it was able to explain some 61% of the variation. Low carbon affinity and growth rate appeared to be a constant feature of the two rosette species. However, species with intermediate carbon affinity, characterized by "end pH" values between 8.8 and 8.9, showed greatly varying growth rates from 0.020 to 0.088 day-1. Moreover, the carbon affinity was not a constant attribute of all species. Growth form and other morphological features are probably more specific, even though they are also under environmental influence. The features used here, however, failed to explain the variation in growth rates. The capacity for lateral and vertical expansion of the shoot (M-index, sensu Kautsky, 1988 ) was also a poor predictor of growth rates (r2=0.10). This was also anticipated since, for example, slow-growing biomass storers and rapidly growing competitors may have similar M-values (Kautsky, 1988 ). The carbon affinity is, therefore, the best predictor of variations in growth rates within this exclusive group of submerged rooted macrophytes of temperate freshwater habitats. ACKNOWLEDGEMENTS

We thank Stephen Maberly and Morten Sondergaard for constructive criticism of the manuscript. We acknowledge financial support by the Danish Research Academy to S.L.N.

GROWTHRATESOF SUBMERGEDROOTEDMACROPHYTES

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REFERENCES Barko, J.W. and Smart, R.M., 1981. Sediment-based nutrition of submersed macrophytes. Aquat. Bot., 10" 339-352. Carignan, R. and Kalff, J., 1980. Phosphorus sources for aquatic weeds: water or sediments. Science, 207: 987-989. Carpenter, S.R. and Lodge, D.M., 1986. Effects of submersed macrophytes on ecosystem processes. Aquat. Bot., 26: 341-370. Chambers, P.A. and Kalff, J., 1985. Depth distribution and biomass of submersed macrophyte communities in relation to secchi depth. Can. J. Fish. Aquat. Sci., 42: 701-709. Duarte, C.M. and Kalff, J., 1986. Littoral slope as a predictor of the maximum biomass of submerged macrophyte communities. Limnol. Oceanogr., 31: 1072-1080. Farmer, A.M. and Spence, D.H.N., 1986. The growth strategies and distribution of isoetids in Scottish freshwater lochs. Aquat. Bot., 26: 247-258. Golterman, H.L. (Editor), 1969. Methods for Chemical Analysis of Fresh Waters (IBP Handbook No. 8 ). Blackwell Scientific, Oxford, 172 pp. Hutchinson, G.E., 1975. A Treatise on Limnology. Vol. 3, Limnological Botany. Wiley, New York, 660 pp. Iversen, T.M., Jeppesen, E., Sand-Jensen, K. and Thorup, J., 1984. Okologiske konsekvenser af reduceret vandforing i Sus~en, bind 1: Den biologiske struktur. Miljostyrelsen, Copenhagen, 91 pp. (in Danish). Kautsky, L., 1988. Life strategies of aquatic soft bottom macrophytes. Oikos, 53:126-135. Kelly, M.G., Thyssen, N. and Moeslund, B., 1983. Light and the annual variation of oxygenand carbon-based measurements of productivity in a macrophyte dominated river. Limnol. Oceanogr., 28:503-515. Kemp, N.M., Murray, L., Borum, J. and Sand-Jensen, K., 1987. Diel growth in eelgrass Zostera marina. Mar. Ecol. Prog. Set., 41: 79-86. Maberly, S.C. and Spence, D.H.N., 1983. Photosynthetic inorganic carbon use by freshwater plants. J. Ecol., 71: 705-724. Madsen, T.V. and Sand-Jensen, K., 1987. Photosynthetic capacity, bicarbonate affinity, and growth of Elodea canadensis Michaux exposed to different concentrations of inorganic carbon. Oikos, 50: 176-182. Norgaard, N., 1989. Vaekst og lysadaptation hos submerse makrofyter. MS Thesis, Botanical Institute, University of Aarhus, 62 pp. (in Danish). Raven, J.A., 1970. Exogenous inorganic carbon sources in plant photosynthesis. Biol. Rev., 45: 167-221. Raven, J.A., 1984. A cost-benefit analysis of photon absorption by photosynthetic unicells. New Phytol., 98: 593-625. Rebsdorf, A., 1972. The carbon dioxide system of freshwater. A set of tables for easy computation of total carbon dioxide and other components of the carbon dioxide system. Freshwater Biological Laboratory, Hillerod, Denmark, unpaginated. Reynolds, C.S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge, 384 pp. Sand-Jensen, K., 1987. Environmental control of bicarbonate use among freshwater and marine macrophytes. In: R.M.M. Crawford (Editor), Plant Life in Aquatic and Amphibious Habitats. Br. Ecol. Soc. Spec. Publ. No. 5, Blackwell Scientific, Oxford, pp. 99-112. Sand-Jensen, K. and Gordon, D.M., 1986. Variable HCO[ affinity of Elodea canadensis Michaux in response to different HCO~- and CO2 concentrations during growth. Oecologia (Berlin), 70: 426-432. Sand-Jensen, K. and Sondergaard, M., 1978. Growth and production ofisoetids in oligotrophic Lake Kalgaard, Denmark. Verh. Int. Ver. Limnol., 20: 659-666. Sand-Jensen, K. and Sondergaard, M., 1979. Distribution and quantitative development of

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aquatic macrophytes in relation to sediment characteristics in oligotrophic Lake Kalgaard, Denmark. Freshwater Biol., 9:1-11. Sand-Jensen, K. and Sondergaard, M., 1981. Phytoplankton and epiphyte development and their shading effect on submerged macrophytes in lakes of different nutrient status. Int. Rev. gesamten Hydrobiol., 66: 529-552. Sand-Jensen, K., Moller, J. and Olesen, B.H., 1988. Biomass regulation of microbenthic algae in a Danish lowland stream. Oikos, 53." 332-340. Sand-Jensen, K., Jeppesen, E., Nielsen, K., van der Bijl, L., Hjermind, L., Nielsen, L.W. and Iversen, T.M., 1989. Growth of macrophytes and ecosystem consequences in a lowland Danish stream. Freshwater Biol., 22:15-32. Sondergaard, M., 1979. Light and dark respiration and the effect of the lacunal system on refixation of CO2 in submerged aquatic plants. Aquat. Bot., 6: 269-283. Sondergaard, M., 1981. Loss of inorganic and organic carbon by MC-labelled aquatic plants. Aquat. Bot., 10: 33-43. Spence, D.H.N. and Maberly, S.C., 1985. Occurrence and ecological importance of HCOj- use among aquatic higher plants. In: W.J. Lucas and J.A. Berry (Editors), Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms. American Society of Plant Physiologists, Rockwell, MD, pp. 125-143. Stumm, W. and Morgan, J.J., 1970. Aquatic Chemistry. An Introduction Emphasizing Chemical Equilibria in Natural Waters. Wiley, New York, 583 pp. Ward, L.G., Kemp, W.N. and Boynton, W.R., 1984. The influence of waves and seagrass communities on suspended particulates in an estuarine embayment. Mar. Geol., 59: 85-103. Wetzel, R.G., 1983. Limnology. 2 Edn. Saunders, Philadelphia, 743 pp. Wetzel, R.G. and Manny, B.A., 1972. Secretion of dissolved organic carbon and nitrogen by aquatic macrophytes. Verh. Int. Ver. Limnol., 18:162-170. Wintermans, J.F.G.M. and DeMots, A., 1965. Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim. Biophys. Acta, 109: 448-453.