SEARCH

SEARCH BY CITATION

Keywords:

  • Cladophora glomerata;
  • acclimation;
  • chlorophyll fluorescence;
  • light-stress;
  • photosynthesis;
  • strategies;
  • temperature;
  • xanthophylls

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES

Cladophora glomerata (L.) Kütz. is the dominant filamentous algae of the river Ilm, Thuringia, Germany. For most of the year it can be found at open as well as at shaded sites. Photosynthetic acclimation of C. glomerata to different light intensities was detected by chlorophyll fluorescence measurements and pigment analysis. Cladophora glomerata from highlight sites showed decreased values of efficiency of open photosystem II (Fv/Fm) as compared with C. glomerata from low-light sites. Winter populations revealed higher Fv/Fm values than summer populations. A light-induced decrease in efficiency of the closed photosystem II was observed at increasing irradiance intensities. The decrease was higher in C. glomerata from shaded sites compared with plants from open sites. Differences in the photosynthetic electron transport rate of different populations of C. glomerata were shown by photosynthesis–irradiance curves. Summer populations from high-light sites yielded higher maximum electron transport rates than plants from low-light sites, whereas winter populations exhibited significantly decreased values compared with the summer populations. Results of the analysis of photosynthetic pigments corresponded with data from chlorophyll fluorescence measurements. In addition to these long-term acclimation effects, C. glomerata expressed its ability to cope with rapid changes in the light environment by the de-epoxidation of violaxanthin during exposure to high light intensities.


INTRODUCTION

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES

Relationships between environmental factors and the dominance of Cladophora glomerata in the Ilm/Thuringia (Germany) has been studied by Ensminger, Hagen & Braune (2000). It became apparent, that not only nutrients play an important role in the formation of C. glomerata-dominated macrophyte assemblages, but also life-cycle properties and the ability to grow under different light conditions. Hence, success of C. glomerata depends on the ability (i) of rapid and frequent dispersal of the population from vegetative cells by zoospores; (ii) to persist in a given habitat even under unfavourable conditions by akinetes; and (iii) to rapidly recolonize a habitat after disturbances. The distribution of C. glomerata is supposed to depend strongly on its ability to handle changing environmental conditions including changes in the light environment. These changes include the seasonal increase and decrease of photosynthetic active radiation (PAR) as well as decreases due to the development of foliage of streamside vegetation. Cladophora glomerata therefore has to cope with high light stress as well as with lower levels of PAR.

Measurements of oxygen production in C. glomerata showed photo-inhibition at irradiances above 500 μmol photons m−2 s−1 ( Dodds 1991). Using fluorescence measurements various authors reported inhibitory effects of high fluence rates on photosynthesis of marine macroalgae ( Hanelt, Hupperts & Nultsch 1993; Uhrmacher, Hanelt & Nultsch 1997; Häder et al. 1997 ). Apart from the effects of excessive fluence rates, Huner, Öquist & Sarhan (1998) demonstrated the relation of cold temperatures to photo-inhibition in unicellular green algae. The mechanism of photo-inhibition is regarded as an active regulatory process to protect the photosynthetic apparatus from excessive radiation, which is accompanied by a decrease of the photosynthetic yield. A central role within this process is given to the turnover of the D1 protein, that is located in photosystem II ( Sundby, McCaffery & Anderson 1993), and the turnover of the protective xanthophyll cycle ( Demmig-Adams, Gilmore & Adams 1996). In marine macroalgae, Uhrmacher et al. (1995) demonstrated the light-induced conversion of the xanthophyll violaxanthin into anthera- and zeaxanthin. Neidhardt et al. (1998) and Masojídek et al. (1999) showed photo-adaptational processes of photosynthetic pigments in unicellular algae in relation to shifts in the light environment.

In freshwater macroalgae little work has been done on the dynamics of photo-inhibition and acclimation of photosynthesis to different light environments as well as to seasonal changes. Leukart & Hanelt (1995) estimated photosynthetic rates of different freshwater macroalgae. From their results they identified typical high-light or low-light species but they did not consider temporal or light-environmental dynamics. Under laboratory conditions various authors studied the effects of light and temperature on photosynthesis of C. glomerata (e.g. Graham et al. 1982 ; Lester, Adams & Farmer 1988).

The present work analyses the response of C. glomerata to different light environments in its dynamic and variable habitat in order to understand strategies that may provide the alga’s success in terms of photosynthesis. At four different sites (i) seasonal differences in the photosynthetic performance of C. glomerata (ii) differences in photosynthetic activity between open and shaded sites, and (iii) plasticity in pigment composition that allows C. glomerata acclimation to different environmental conditions were studied. On the basis of the data obtained we determined the main factors that have strong impact on the photosynthetic efficiency of C. glomerata in the Ilm.

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES

Study sites

A brief description of the Ilm is given in Ensminger et al. (2000). Two locations in the metarhithral of the river were selected for observation. One location was situated upstream and the second downstream of the town Stadtilm. Sampling of algae for pigment analysis and measurements of chlorophyll fluorescence were undertaken from May 1997 to May 1998. If C. glomerata was available, samples were taken at each location at 14 d intervals from one open site (exposed to full sunlight and therefore referred to as high-light or HL site) and one shaded site (characterized by seasonally varying degrees of shade due to streamside vegetation and therefore referred to as low-light or LL site). As samples from deep in a large tuft could experience lower light than those taken from the surface, we took only upper filaments from the final 5 cm of the apical thallus end.

Chlorophyll fluorescence

A portable fluorometer (PAM-2000; Walz, Effeltrich, Germany) was used to perform measurements of chlorophyll fluorescence of C. glomerata under natural sunlight in situ under water. A self-constructed device allowed exposure of the filamentous algal thalli during determination of optimum quantum yield [Fv/Fm = (FmF0)/Fm], which is a measure of the efficiency of open photosystem II units (PSII), and during determination of effective quantum yield [ΔF/Fm′ = (Fm′–Ft)/Fm′], as a measure of the efficiency of closed PSII units ( Schreiber, Bilger & Neubauer 1994). First, effective quantum yield was probed by measurement of saturating flash-induced maximal fluorescence (Fm′) of the sample adapted to natural sunlight. Optimum quantum yield was determined after subsequent 5 min pre-darkening of the same sample by detection of (i) dark-adapted basic fluorescence (F0) under weak red modulated light (approximately 0·18 μmol photons m−2 s−1) and (ii) maximal fluorescence (Fm) during a 600 ms flash of white light (approximately 6000 μmol photons m−2 s−1). Light-induced relative decrease of the effective quantum yield was calculated as r(ΔF/Fm′)* = 100–(100 ×ΔF/Fm′/(Fv/Fm)).

Simultaneously with determination of effective quantum yield, incident PAR was measured close to the algal sample with a Li-192 (Li-Cor, Lincoln, NB, USA) underwater quantum sensor connected to the PAM-2000. Photosynthesis was expressed as relative electron transport rate (rETR) and was calculated as rETR = PAR ×ΔF/Fm′× 0·5 ( Genty, Briantais & Baker 1989). The values of rETR obtained were used to calculate photosynthesis–irradiance curves (P–I curves). Instead of the use of artificial light sources or filters, and in order to obtain different irradiance levels, data of repeated rETR measurements were used from different sampling dates combined with incident PAR measured simultaneously during the estimation of ΔF/Fm′. The steady-state rETR of the samples, obtained in this manner, was calculated from measurements of 17 different sampling days during summer (April to September) and 11 sampling days during winter (October to March). These rETR data were first grouped into plants from open and from shaded sites, and afterwards each light condition was further divided into groups of summer and winter plants. Characteristic parameters of the P–I curves ( Henley 1993) are light-saturated photosynthetic rate (Pmax), initial slope of the non-saturated photosynthetic rate (αI), and optimum light intensity (Ik, that indicates the beginning of light-saturated photosynthesis). These parameters were derived from least-square fits of the data to a model described by Eilers & Peeters (1988).

As rETR values are a ratio of fluorescence values, they are independent of biomass and can be compared across season.

Pigment analysis

Samples of C. glomerata (0·2–0·5 g fresh-weight) were rinsed several times in river water to remove loosely attached epiphytes and sediment. Then, samples were rinsed with distilled water, dry blotted for 20 s between four layers of filter paper and immediately deep-frozen in liquid nitrogen. In the laboratory, the deep-frozen samples were homogenized with a mixer mill (Retsch, Haan, Germany), and pigments were extracted in 100% acetone under dim-light conditions at 4 °C. Pigment content was determined spectrophotometrically according to Lichtenthaler (1987). The pigment pattern was further analysed by high-performance liquid chromatography (HPLC) using the same extracts after addition of 15% H2O ( Büch et al. 1994 ; Xyländer, Hagen & Braune 1996). As epiphytic diatoms could not entirely be removed during the cleaning and homogenization procedure, the amount of diatomic chlorophyll a (Chl a) was calculated from the amount of Chl c per sample. A fixed molar Chl a to Chl c ratio of 5·3 from our own laboratory measurements was taken as a basis and the calculated value was subtracted from the total amount of Chl a.

Statistics

The software package SPSS release 9·0 (SPSS, Chicago, IL, USA) was used to perform statistical tests and procedures.

RESULTS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES

Quantum efficiency of open PSII of C. glomerata

For pooled data that covered the whole sampling period, the measurements of optimum quantum efficiency (Fv/Fm) did not show significant differences among the four sites or between the upstream and downstream locations (one-way ANOVA, data not shown). In contrast, grouping of data from open and shaded sites into summer and winter populations revealed seasonal differences as well as differences in dependence on light conditions. Samples of HL summer populations exhibited decreased Fv/Fm-values in comparison with LL plants that were experimentally exposed for 8 min to full sunlight ( Fig. 1). After 8 min of exposure to shade conditions before subsequent dark adaptation and measurement of Fv/Fm, a significant recovery from 0·649 to 0·693 (t-test, P < 0·05) was observed in HL plants. However, the values were still lower in comparison with plants from shaded sites. During winter, the maximal photosynthetic capacity of all samples was increased in comparison with summer. The pattern of lower values in HL and higher values in LL plants was still observed ( Fig. 1). The difference between HL and LL winter populations was significant and higher in comparison with the summer populations (t-test, P < 0·05). After exposure to shade, HL and LL winter plants also exhibited increased values of Fv/Fm, as shown above in summer populations.

image

Figure 1. Differences in efficiency of open PSII in C. glomerata from open sites (HL) and from shaded sites (LL) after exposure to full sunlight and shade.

Download figure to PowerPoint

Light-induced decrease of effective quantum yield

A light-induced decrease of the effective quantum yield was observed in HL and LL summer plants of C. glomerata ( Fig. 2). At low irradiance levels (< 200 μmol photons m−2 s−1), the light-induced decrease of ΔF/Fm′ was almost the same in HL and in LL plants. Increased irradiance levels resulted in pronounced light-induced decreases of r(ΔF/Fm′)* in all plants, but the decrease was higher in LL compared with HL plants.

image

Figure 2. Light-induced decrease of the effective quantum yield of PS II in C. glomerata from open (○, dotted line) and from shaded (●, full line) sites between April and September.

Download figure to PowerPoint

Differences in characteristics of photosynthesis–irradiance curves

Values of effective quantum yield were used to calculate rETR ( Fig. 3). Data were analysed for seasonal and site-specific differences. In summer populations of C. glomerata from both open and shaded sites, no differences were observed in the effectivity of rETR at non-saturating irradiances. This was indicated by values of 0·318 and 0·381 of the initial slope αI for HL and LL plants, respectively ( Fig. 3a, Table 1). At higher irradiance levels, C. glomerata from open sites showed higher values of rETR and a higher saturation factor Ik as compared with plants from shaded sites. This pattern was sharply contrasted by light-saturation characteristics of rETR in winter populations of C. glomerata ( Fig. 3b, Table 1). The P–I characteristics of HL and LL plants were almost identical. The initial slope αI increased in winter in comparison with summer populations, whereas rETRmax decreased to almost identical values of 43·21 and 40·87 in HL and LL plants ( Fig. 3b, Table 1). Similarly, the saturation factor IK dropped to values of 96·67 (HL) and 99·93 (LL).

image

Figure 3. Differences in photosynthesis-irradiance-characteristics of summer (a) and winter populations (b) of C. glomerata from open and shaded sites. Each data point represents the mean of five to seven measurements ± SE.

Download figure to PowerPoint

Table 1.  Characteristic parameters of photosynthesis–irradiance-curves of C. glomerata
  αIrETRmaxIK (μmol m−2 s−1) Rmn
  1. αI = initial slope of the photosynthetic rate, rETRmax = maximum relative electron transport rate, IK = light saturation factor (= rETRmaxαI−1), Rm = multiple correlation coefficient, n = number of samples.

SummerOpen sites0·318110·17346·450·970215
 (± asymptotic SE)0·0324·0437·11
 Shaded sites0·38182·94217·690·95398
 (± asymptotic SE)0·0606·8438·70
WinterOpen sites0·44743·2196·670·916180
 (± asymptotic SE)0·0722·1316·28
 Shaded sites0·40940·8799·930·86175
 (± asymptotic SE)0·1443·6410·70

Changes in photosynthetic pigments

Seasonal and light-dependent variations in the photosynthetic pigment pattern of C. glomerata were detected spectrophotometrically and by HPLC analysis ( Fig. 4). Higher concentrations of Chl a and Chl b were found during summer in HL and LL plants compared with the winter populations ( Fig. 4a, P < 0·05 for each group). Whereas in summer the Chl content in LL plants exceeded that in HL plants, the Chl content of LL winter plants was lower than in HL plants. For the whole sampling period, as well as for summer and winter populations, the ratio of Chl a to Chl b was significantly higher in C. glomerata from open sites compared with plants from shaded sites ( Fig. 4b, t-test, P < 0·05), significant seasonal differences were not found.

image

Figure 4. Seasonal changes in pigment composition of summer (open bars) and winter populations (filled bars) of C. glomerata from the Ilm. Total chlorophyll (a), chlorophyll a per chlorophyll b (b), carotenoids per total chlorophyll (c), xanthophylls per total chlorophyll (d), de-epoxidation state of xanthophylls (e).

Download figure to PowerPoint

The ratio of carotenoids to chlorophylls reflected higher carotenoid levels during winter in HL as well as in LL plants compared with the summer ( Fig. 4c, t-test, P < 0·05). Only during summer did HL plants contain higher amounts of carotenoids than LL plants (t-test, P < 0·05), whereas in winter the HL and LL plants showed equal values ( Fig. 4c, t-test, NS). The ratio of the xanthophyll cycle pigments (VAZ), namely violaxanthin (V), antheraxanthin (A) and zeaxanthin (Z), per Chl a + Chl b was higher in HL summer populations than in HL winter populations (t-test, P < 0·05), whereas in LL plants a seasonal difference was not found and the ratio remained constant ( Fig. 4d).

For the whole sampling period, the de-epoxidation state of the xanthophyll cycle pigments (0·5 A + Z)/(V + A + Z) was higher in HL than in LL plants ( Fig. 4e, t-test, P < 0·05). For HL plants the seasonal comparison of the conversion state revealed higher summer values (t-test, P < 0·05) but in LL plants there was no significant difference between summer and winter samples. The HL summer plants showed a higher conversion state than LL plants, but during winter no significant difference between HL and LL plants appeared.

Analysis of factors determining the photosynthetic efficiency of C. glomerata

Univariate analysis of variance was used to identify relationships between important environmental factors and the Chl fluorescence yield parameter ΔF/Fm′, that indicates photosynthetic efficiency of C. glomerata under ambient light conditions. For this procedure photosynthetic active radiation (PAR, data not shown) at the algal surface during the determination of ΔF/Fm′ was used in addition with physical and chemical-parameters water temperature, oxygen saturation, conductivity, pH, global irradiance, effective irradiance, current velocity, NH4+-N, NO3-N, and soluble reactive phosphorus as well as mean, maximum and minimum discharge rate (for datasets see Ensminger et al. 2000). A general linear model (GLM) with a forward selection method was applied to test all kinds of cross-relations between the measured parameters. From this complete set of physical and chemical parameters only PAR and water temperature were found to have statistically significant effects on the photosynthetic efficiency (P < 0·01). A quantitative description of this relationship was achieved by using a random selection of 50% of the observed cases of the ΔF/Fm′ data of C. glomerata to estimate a multiple regression model ( Fig. 5). The accuracy of the model was tested with the remaining 50% of the cases. The predicted ΔF/Fm′ values of C. glomerata were calculated on the basis of the corresponding PAR and water temperature data and were plotted against the observed values ( Fig. 5). The accuracy of the model is expressed by the R-squared value, R2 = 0·76, of the linear regression line.

image

Figure 5. Relationship between observed and predicted values of photosynthetic efficiency of C. glomerata by the multiple regression model ΔF/Fm′ = 0·522 – (IA× 0·00049) + (TH2O× 0·00918); IA = actual PAR during determination of effective quantum yield; TH2O = water temperature. Regression ANOVAP < 0·05. The accuracy of the fit is given as R2 = 0·76.

Download figure to PowerPoint

DISCUSSION

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES

Seasonal differences of the photosynthetic performance of C. glomerata

The optimum quantum yield given as the ratio of variable to maximal fluorescence (Fv/Fm) is a good parameter to illustrate changes in the efficiency of open PSII centres ( Schreiber et al. 1994 ). It is widely used to assess effects of light on photosynthesis, to reflect photo-inhibition and processes related to the activity of the xanthophyll cycle, and thus, allows the estimation of light stress and the regulation of photosynthetic energy conversion of PSII (e.g. Schreiber et al. 1994 ; Masojídek et al. 1999 ).According to this the results given in Fig. 1 reveal different degrees of photo-inhibition in C. glomerata. During summer, exposure of C. glomerata to full sunlight resulted in decreased Fv/Fm values due to excessive light. Patterns of recovery, indicated by increased values, were observed after short-time recovery under shade conditions. This revealed photo-inhibitory up- and down-regulation of PSII efficiency. This pattern was also apparent during winter when the observed irradiance levels amounted only 10–20% of the values observed during April to September. Huner et al. (1998) and Ottander et al. (1993) discussed photosynthesis and its inhibition not only in terms of light stress but also in relation to cold temperatures. Energy imbalances between the light energy absorbed through photochemistry versus energy utilized through metabolism are considered to cause over-excitation of PSII and thus, photo-inhibition. Low-temperature acclimation, that was assumed for winter populations of C. glomerata, therein resulted in the observed depression of photosynthetic efficiency after exposure to full winter sunlight.

Differences of photosynthetic parameters at open and at shaded sites

Cladophora glomerata from open and from shaded sites revealed different abilities to regulate the quantum efficiency of PSII to provide protection of the photosystem from damage due to excessive photon fluence rates ( Fig. 2). The HL plants possessed a higher capacity to cope with high irradiance levels, as indicated by the higher percentage values of the light-induced decrease of ΔF/Fm′ relative to Fv/Fm. At low irradiance levels, HL plants already revealed slightly decreased values compared with LL plants. These results coincided with the increased levels of carotenoids and xanthophyll cycle pigments observed in HL plants, as is discussed below. Thus, the less efficient use of the light resource by HL plants exhibited the properties of a photosystem that was used to dealing with superfluously high fluence rates. The lesser light-induced decrease of ΔF/Fm′ at low light intensities, that was revealed by LL plants, accounted for their acclimation to low fluence rates and the need to make efficient use of the limited light resource. At fluence rates higher than 200 μmol m−2 s−1, a higher decrease further reflected that these plants were not optimized to deal with high fluence rates ( Fig. 2). Again, these results were related to carotenoid and xanthophyll cycle levels in the samples, as LL plants did not need to make intensive use of the protective and regulatory properties of these pigments (see below). These differences in light-induced decrease of photosynthetic efficiency between plants from open and from shaded sites indeed demonstrate the ability of C. glomerata to develop different capacities of energy conversion in PSII, depending upon its light environment.

Acclimation to seasonal changes of environmental conditions were further shown in the P–I curves ( Fig. 3). During summer, the P–I characteristics differed between HL and LL plants ( Fig. 3a). The values of Ik and rETRmax were higher in C. glomerata from open sites compared with plants from shaded sites and thus illustrated the acclimation of the HL plants to high fluence rates ( Table 1). Winter plants strongly reflected seasonal changes of environmental conditions. Lower temperature and irradiance levels and lower irradiance maxima in addition to less pronounced differences of the light regime between open and shaded sites resulted in changes of the photosynthetic efficiency of C. glomerata ( Fig. 3b, Table 1). During winter the values of rETRmax and Ik strongly decreased and there were no longer any differences between HL and LL plants, together indicating the down-regulation of photosynthesis. Higher αI-values in comparison with summer expressed the acclimation to low irradiance levels and the effective energy conversion under these light conditions.

The model that was used to calculate the P–I curves did not detect any photo-inhibition, as it would be indicated by a negative slope at supersaturating irradiance levels. This is presumably due to sampling and immediate measurement under natural light conditions. Thus, samples reflected steady-state performance of the photosynthetic apparatus. This handling avoided cumulative effects by measurements at increasing irradiance steps, as it usually occurs in P–I experiments ( Henley 1993). It does not imply that there was no inhibition of photosynthetic rates at all. As Henley (1993) pointed out, that patterns of photo-inhibition are time dependent and P–I changes encompass several mechanisms, most of them are better classified as photoregulation/protection or dynamic photo-inhibition rather than damage to PSII ( Krause & Weis 1991). Hence, only after prolonged exposure to supersaturating irradiances, might the maximum photosynthetic rate, as well as the saturation constants, show a decrease. In this respect, the implication of our results is that PSII electron transport capacity exceeds carboxylation capacity at saturating irradiances until a critical percentage of PSII centres have been de-activated. Thereafter, photosynthetic rate is limited by PSII electron transport at all irradiances ( Henley 1993). This is consistent with the observed decline of rETRmax in summer LL compared to summer HL samples, and in winter compared with the summer samples.

Plasticity in pigment composition allows acclimation to different light regimes

The changes in photosynthetic efficiency were concomitant with the changes in pigment composition. Acclimation to low-light environments was shown by increased amounts of Chl per dryweight in summer C. glomerata from shaded sites ( Fig. 4a). The lower values observed in winter plants from shaded and from open sites may be due to two different processes: (a) under low-light conditions and cold temperatures C. glomerata is able to form resting cells. That is accompanied by degradation of chlorophylls and the formation of thicker cell walls. This process, of course, influences the ratio of Chl/dry weight. Thus, during winter occasionally dark-green and brownish-appearing filaments were found; and (b) the photosynthetic apparatus acclimates to different environmental conditions by varying the amount of Chl. In this way C. glomerata seems to down-regulate its light-capture efficiency in an unfavourable environment. Higher Chl a to Chl b ratios in LL plants during summer as given in Fig. 4b were mainly due to higher amounts of Chl b. Localized in the antenna complex, Chl b increases the absorption efficiency of the photosystem and indicates the acclimation of the photosystem of the algae to shade conditions. Such increases in the amount of Chl b were shown in unicellular green algae, that were converted from HL to LL growth conditions, for example, by Berner et al. (1989) . In contrast, in winter, when biochemistry, not photochemistry, is limited by low ambient temperatures, it might be useful to reduce the absorption efficiency in HL as well as in LL plants ( Huner et al. 1998 ). This will minimize photo-inhibition and potential damage from irradiance levels that result from excessive excitation energy under cold temperatures. The overall increase in carotenoids per Chl as shown in Fig. 4c emphasizes the above-mentioned, as it indicates two important changes in pigmentation, the reduction of the total amount of Chl and an increase of carotenoids that serve as a protective agent to increase heat dissipation of absorbed energy ( Demmig-Adams et al. 1996 ). Further, acclimation to light stress is indicated in Fig. 4d by the increased xanthophyll pool size in HL compared to LL summer plants. Acclimation to cold temperatures is expressed by the high levels of xanthophylls in winter plants from both open and shaded sites. It becomes obvious that in HL plants in summer and in HL and LL plants in winter, increased VAZ levels serve to protect the antenna from over excitation. The use that C. glomerata makes of this protective energy-dissipating system is well illustrated in Fig. 4e by higher de-epoxidation levels in summer in HL plants compared with LL plants.

Taken together, the observed change of pigment composition in response to growth at low temperatures or high irradiances results in a reduction in light-harvesting capacity together with an increased capacity to dissipate excess light as heat through carotenoids and the xanthophylls, antheraxanthin and zeaxanthin.

Factors determining photosynthetic efficiency of C. glomerata

The linear regression formula suggests that photosynthetic efficiency of C. glomerata was mostly effected by PAR and water temperature ( Fig. 5). As it was shown in Fig. 2, ΔF/Fm′ decreases at increasing light intensities, and thus, explains the negative regression coefficient found for PAR. In addition, positive effects of an increase in water temperature, as suggested by the positive regression coefficient, indicate the importance of a balanced energy flux. At cold temperatures photochemical reactions are slowed down and photosynthetic efficiency has to be reduced to avoid photodamage. This reduction of photosynthetic efficiency depends on the pigmentation of C. glomerata and was shown to be evident in Fig. 4.

The quality of the model is given by the R-squared value, R2 = 0·76 ( Fig. 5). It shows that reasonable estimates can be obtained from the regression equation. In fact, there are still factors that have not been included in the analysis, but which potentially account for unexplained variations of photosynthetic efficiency. Amongst these are for instance different levels of vitality of algal samples due to different cell ages, or stress caused by pulses of saline effluents (Ensminger et al. 2000, this issue).

In conclusion, the results demonstrate the complexity of the influences of environmental factors on photosynthetic activity of C. glomerata. Considering the properties of its life cycle (cf. Ensminger et al. 2000), the plasticity of the photosynthetic apparatus allows the acclimation to different habitat conditions, and might provide an important advantage compared with species without these abilities. It is the aim of future studies to focus on differences in ecophysiology of photosynthesis of C. glomerata and other macroalgae.

ACKNOWLEDGMENTS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES

This study was supported by grants of the Deutsche Forschungsgemeinschaft (DFG) Graduate Study Group Analysis of Function and Regeneration of Degraded Ecosystems (Förderkennzeichen GRK 266/1–96). Data on discharge and nutrients were kindly provided by Staatliches Umweltamt Erfurt. Deutscher Wetterdienst Offenbach provided data on global irradiance. Two anonymous reviewers provided helpful suggestions on the manuscript. Erica Froneberg (Vienna) kindly gave valuable comments on the English draft.

REFERENCES

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  • Berner T., Dubinsky Z., Wyman K., Falkowski P.G. (1989) Photoadaption and the ‘package’ effect in Dunaliella tertiolecta (Chlorophyceae). Journal of Phycology 25, 70 78.
  • Büch K., Stransky H., Bigus H.J., Hager A. (1994) Enhancement by artificial electron acceptors of thylakoid lumen acidification and zeaxanthin formation. Journal of Plant Physiology 144, 641 648.
  • Demmig-Adams B., Gilmore A.M., Adams W.A. (1996) In vivo functions of carotenoids in higher plants. FASEB Journal 10, 403 412.
  • Dodds W.K. (1991) Community interactions between the filamentous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and epiphyte grazers. Oecologia 85, 572 580.
  • Eilers P.H.C. & Peeters J.C.H. (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modeling 42, 199 215.
  • Ensminger I., Hagen C., Braune W. (2000) Strategies providing success in a variable habitat: I. Relationships of environmental factors and dominance of Cladophora glomerata. Plant, Cell and Environment 23, 1119 1128.
  • Genty B.E., Briantais J.M., Baker N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87 92.
  • Graham J.M., Auer M.T., Canale R.P., Hoffmann J.P. (1982) Ecological studies and mathematical modeling of Cladophora in Lake Huron: 4. Photosynthesis and respiration as functions of light and temperature. Journal of Great Lakes Research 8, 100 111.
  • Häder D.P., Herrman H., Schäfer J., Santas R. (1997) Photosynthetic fluorescence induction and oxygen production in two Mediterranean Cladophora species measured on site. Aquatic Botany 56, 253 264.DOI: 10.1016/s0304-3770(96)01107-2
  • Hanelt D., Hupperts K., Nultsch W. (1993) Daily course of photosynthesis and photoinhibition in marine macroalgae investigated in the laboratory and field. Marine Ecology Progress Series 97, 31 37.
  • Henley W.J. (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. Journal of Phycology 29, 729 739.
  • Huner P.A., Öquist G., Sarhan F. (1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224 230.DOI: 10.1016/s1360-1385(98)01248-5
  • Krause G.H. & Weis E. (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 13 49.
  • Lester W.W., Adams M.S., Farmer A.M. (1988) Effects of light and temperature on photosynthesis of the nuisance alga Cladophora glomerata (L.) Kutz from Green Bay, Lake Michigan. New Phytologist 109, 53 58.
  • Leukart P. & Hanelt D. (1995) Light requirements for photosynthesis and growth in several macroalgae from a small soft-water stream in the Spessart-Mountains, Germany. Phycologia 34, 528 532.
  • Lichtenthaler H.K. (1987) Chlorophylls and carotenoids – pigments of photosynthetic biomembranes. Methods in Enzymologie 148, 350 382.
  • Masojídek J., Torzillo G., Koblíˇzek J., Kopeck´y J., Bernardini P., Sacchi A., Komenda J. (1999) Photoadaptation of two members of the chlorophyta (Scendesmus and Chlorella) in laboratory and outdoor cultures: changes in chlorophyll fluorescence quenching and the xanthophyll cycle. Planta 209, 126 135.DOI: 10.1007/s004250050614
  • Neidhardt J., Benemann J.R., Zhang L., Melis A. (1998) Relationship between chronic photoinhibition, light-harvesting chlorophyll antenna size and photosynthetic productivity in Dunaliella salina (green algae). Photosynthesis Research 56, 175 184.
  • Ottander C., Hundall T., Andersson B., Huner P.A., Öquist G. (1993) Photosystem II reaction centres stay intact during low temperature photoinhibition. Photosynthesis Research 35, 191 200.
  • Schreiber U., Bilger W., Neubauer C. (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In Ecophysiology of Photosynthesis (eds E.D. Schulze & M.M. Caldwell), pp. 49 70. Springer-Verlag, Berlin.
  • Sundby C., McCaffery S., Anderson M. (1993) Turnover of the photosystem II D1 protein in higher plants under photoinhibitory and nonphotoinhibitory irradiance. Journal of Biological Chemistry 268, 25476 25482.
  • Uhrmacher S., Hanelt D., Nultsch W. (1997) Zeaxanthin content and the degree of photoinhibition are linearly correlated in the brown alga Dictyota dichotoma. Marine Biology 123, 159 165.
  • Xyländer M., Hagen C., Braune W. (1996) Mercury increases light susceptibility in the green alga Haematococcus lacustris. Botanica Acta 109, 222 228.