TY - JOUR
AU - Braune, Wolfram
AB - Abstract The small-scale distribution pattern of macroalgae in the river Ilm, in Germany was monitored. These patterns were then related to abiotic factors and tested to discover whether the distribution of the common macroalgae, Cladophora glomerata (L.) Kütz. and Vaucheria sp., was linked to differences in their photosynthetic plasticity. Cladophora glomerata revealed higher maximum photosynthetic electron transport rates after acclimation to high light (HL) compared with low light (LL) acclimated samples. By contrast, Vaucheria sp. did not acclimate to different growth light conditions. The photosynthetic performance of both algae also varied according to diurnal conditions. High light caused a reversible decrease of the dark-adapted quantum yield (Fv/Fm) in C. glomerata and a concomitant reversible decrease of the light-adapted quantum yield \(({\Delta}F/F{^\prime}_{\mathrm{m}}).\) In Vaucheria sp., Fv/Fm remained mostly unchanged over the day, whereas \({\Delta}F/F{^\prime}_{\mathrm{m}}\) decreased during the morning at low light. Photosynthetic pigments confirmed acclimational differences between the species. HL C. glomerata showed increased chlorophyll a:chlorophyll b ratios, and higher amounts of xanthophyll-cycle pigments compared with LL samples, whereas Vaucheria sp. did not reveal differences between the light treatments. While preferences for substrate size, water velocity, and depth are similar for C. glomerata and Vaucheria sp., the physiological responses to light conditions are different. It is concluded that light conditions significantly affect the small-scale spatial distribution of macroalgae and that fitness is enhanced in species with a higher plasticity in photosynthetic acclimation in unstable environments. Electron transport, environmental conditions, freshwater algae, photoinhibition, spatial distribution, xanthophyll cycle Introduction In freshwater ecosystems, the distribution of benthic algae is caused by proximate, intermediate, and ultimate factors in a complex, hierarchical system (Stevenson, 1997). Ultimate factors such as climate and geology influence the distribution of benthic macroalgae on a large spatial scale (Thiébaut and Muller, 1998), whereas proximate factors (i.e. those directly affecting metabolism and function of the organisms) structure the community on a small spatial scale. Proximate factors, such as discharge rates or light conditions, are constantly changing in stream habitats. The capacity for morphological, physiological, or life-history modifications, usually termed phenotypic plasticity, enables species to respond to these changing environmental factors. This response is reflected in the actual acclimation and thus the adjustment of processes or structures on time-scales less than one generation. Phenotypic plasticity therefore enhances the probability of survival and hence the fitness of an organism, and affects species distribution. Following Stevenson (1997), discharge rates, and physical and chemical properties of the water-body were chosen as the proximate factors in this study and their effect on the distribution of benthic macroalgae was examined on a small spatial scale. Other important proximate factors considered here include (i) substratum size: bigger stones and blocks tend not to be turned over by the current as easily as smaller stones and pebbles and thus offer more stable conditions for the settlement of or shelter for algae (Power and Stewart, 1987; Francoeur et al., 1998). This is particularly true for Cladophora sp. and for Rhizoclonium sp., for which a positive correlation between the size of the substratum and its abundance was demonstrated (Power and Stewart, 1987; Dodds and Gudder, 1992). (ii) Water velocity: the current provides nutrients, and CO2 and \(\mathrm{HCO}_{3}^{{-}}\) as substrates for photosynthesis. On the other hand, increased current can also mechanically stress and tear off algae (Biggs, 1996; Stevenson, 1997). For Cladophora sp., Schönborn (1996) found maximum growth rates at water velocities between 0.5 and 0.8 m s−1. (iii) Light conditions: light capture is crucial for photoautotrophs to be able to maintain metabolism. Photosynthesis of plants and algae responds to changes in growth conditions by a dynamic process known as photosynthetic acclimation (Walters, 2005). It serves to reverse the consequences of environmental change in order to maintain a homeostasis between light capture and the metabolic energy demands of the organism (Huner et al., 1998; Walters, 2005). Therefore photosynthetic acclimation serves not only to maximize photosynthetic gain but also to protect photosynthesis from excess light, which otherwise can result in photoinhibition and can chronically impair photosynthesis (Krause, 1988; Osmond, 1994; Franklin and Forster, 1997). Photosynthetic organisms have evolved a number of protective mechanisms against photo-oxidative damage caused by excess light (Niyogi, 1999; Cruz et al., 2005). One important mechanism is the non-photochemical quenching of excess energy via heat. This involves the rapid conversion of violaxanthin into anthera- and zeaxanthin under high-light conditions in higher plants (Demmig-Adams and Adams, 1992; Horton et al., 1994; Haveaux et al., 2004) or green algae (Masojidek et al., 2004). In some algal taxa, this process involves the light-dependent conversion of diadino- into diatoxanthin (Olaizola and Yamamoto, 1994). Species distribution in the field has been suggested to be associated with photoinhibitory processes (Long et al., 1994), which might be especially true for macroalgae (Franklin and Forster, 1997). In marine arctic algae, for example, depth distribution was related to their capacity for dynamic photoinhibition (Hanelt, 1998), and Silva et al. (1998) observed differences in the light responses of photosynthesis in the marine red alga Gelidium sesquipedale at different depths. Benthic freshwater algae grow in an environment whose incident light intensity varies over the course of the year due to sun angle change and the seasonal changes in the canopy properties of deciduous riparian vegetation. Changes in benthic algal distribution might therefore reflect specialized traits and species' ability to cope with certain light conditions. It is therefore possible to separate sun from shade species in laboratory experiments by analysing physiological parameters (Leukart and Hanelt, 1995). On the other hand, Ensminger et al. (2000) observed acclimation to different light environments in C. glomerata (L.) Kütz. over the course of a year and in relation to the growth light conditions in the natural habitat. No information on the phenological plasticity of other benthic freshwater algae or on their capacity to acclimate to the naturally changing light environment is available. However, the seasonal acclimation of photosynthesis to a naturally changing light environment has recently been shown to be a factor promoting the invasion of Caulerpa racemosa var. occidentalis in coastal Mediterranean areas (Raniello et al., 2004). There is a suggestion that, in different species, different strategies of photosynthetic light utilization exist which might be linked to species succession in different seasons and their small-scale distribution. Therefore, in addition to monitoring the observed species distribution, a physiological approach was used to assess phenotypic plasticity in algae and their ability to acclimate photosynthetically to different light conditions. For this purpose, C. glomerata, the dominant species in the river Ilm, was chosen, together with Vaucheria sp. which belongs to a different algal division and represents a different organization of the photosynthetic apparatus (see below). Both species form characteristic algal mats and are common in temperate streams. Materials and methods Study site The Ilm is a small mountain river with headwaters in the ‘Thüringer Wald’ in Thuringia, Germany. All research was done in the hyporhithral of the Ilm. To assess the effect of different light conditions on the algae, two different kinds of sites were investigated: shaded ones (low light, LL), which were bordered by trees, and open sites without riparian vegetation, which were exposed to full sunlight (high light, HL). The typical range of PPFD (photosynthetic photon fluence density) on a clear day during July was about 1200 μmol photons m−2 s−1 at open sites and about 200 μmol photons m−2 s−1 at shaded sites (Ensminger et al., 2001). To obtain physiological measurements, algal patches were taken from open sites in the stream and kept for 10–14 d in flow-through channels. The channels were set up in an empty basin of a trout hatchery. Water was supplied directly from the Ilm by the water distribution system of the hatchery. Water velocity was kept at about 0.5 m s−1 by adjusting the slope of the channels. The experimental channels were similar to field sites with respect to light. Black nylon mesh was used to cover the channels in order to create shaded habitats where algae received only 40% (two layers of nylon mesh) or 20% (four layers of nylon mesh) of the incident PPFD. Distribution of macroalgae Twenty transects were established across the stream, along a 1 km stretch in the hyporhithral of the river Ilm upstream of the village of Buchfart. Transects included open as well as shaded sites and sites of different depths (up to 0.8 m). Macroalgae were monitored at 1 m intervals along each transect using a glass-bottom viewing device (0.2 m diameter of the field of view). In addition to the macroalgae, the moss Fontinalis antipyretica (L.) was included in the monitoring and in the statistical analysis, as it occurs exclusively on bigger stones and boulders and thus might compete with the algae for the most stable substratum at the study site. Algae were determined to at least the level of genus, and the percentage of cover per view was estimated. The presence of diatoms was noted when they formed macroscopically visible mats. For C. glomerata, the maximum length of thalli was estimated to the nearest 0.1 m. Water velocity was measured at 1 m intervals and about 0.03 m above the bottom using a portable Flow-Meter (Marsh-Mc Birney Inc., USA). The type of substratum was monitored on a 6-step scale (Schönborn, 1992): 1=sand, 2=small gravel <5 cm, 3=medium-sized gravel 5–10 cm, 4=coarse gravel >10–15 cm, 5=stones >15–20 cm, 6=boulders >20 cm. The light conditions were estimated on the following 5-step scale: 5=100% irradiance, completely open site; 4=80% irradiance, mostly open, receives sunlight during most of the day; 3=60% irradiance, receives sunlight for about half of the day; 2=40% irradiance, shaded throughout most of the day, 1=20% irradiance, completely shaded. The daily discharge rates as measured about 5 km downstream of the experimentation site were provided by Staatliches Umweltamt Erfurt. Data of the daily sum of irradiance were provided by Deutscher Wetterdienst Offenbach (DWD) from the nearest station at Weimar. Relative levels of irradiance were calculated as a simple measure, reflecting differences in typical growth light conditions over a period of one week. This simple but meaningful parameter was derived from the weekly average of the daily sum of irradiance. The average value was then weighed for each single sampling point according to the classified 5-step scale for the light conditions (see above) to obtain the relative level of irradiance. Iron poles were used to mark the transects permanently and mapping was repeated on a weekly basis during the spring and summer of 1999 in order to assess the extent of seasonal variation and the impact of disturbances/flooding events. Sixteen mapping days with 20 transects resulted in a total of 2772 observations. Water temperature (°C), conductivity (mS m−1), pH, O2-content (g m−3), and O2-saturation (%) were assessed weekly at the centre of the transects with a universal meter (WTW, Germany), and the concentration of \(\mathrm{NO}_{2}^{{-}},\) \(\mathrm{NO}_{3}^{{-}},\) \(\mathrm{NH}_{4}^{{+}},\) and \(o-\mathrm{PO}_{4}^{{-}}\) in the water column was determined using Merck equipment (Merck, Germany). Photosynthetic activity of C. glomerata and Vaucheria sp. Differences in photosynthetic activity were assessed in situ via chlorophyll fluorescence using a portable pulse-modulated system (PAM-2000, Walz, Effeltrich, Germany). A custom-designed clip was used to hold the algal sample in the flowing water during measurements. Photosynthetic performance was determined by measuring photosynthesis–irradiance curves (P−I curves). Samples of C. glomerata and Vaucheria sp. were taken from HL- and LL-treatments from the flow-through channels early in the morning before they experienced over-excitation from high-incidence sunlight. Only filaments that appeared to be free of epiphytic diatoms after visual inspection were used for fluorescence measurements. A programmed computer routine for the PAM-2000 was used for the following measuring scheme: after 5 min of pre-darkening and application of 20 s of far-red light (λ=700 nm), the optimum quantum yield (as Fv/Fm=(Fm−Fo)/Fm, after van Kooten and Snel, 1990) was calculated using the basic fluorescence F0 and the maximum fluorescence Fm obtained after application of a completely saturating white light flash (∼6000 μmol m−2 s−1). Following this, the sample was illuminated with actinic white light, whose intensity was increased stepwise every 40 s from 10 to about 800 μmol photons m−2 s−1 of PPFD. After 40 s of illumination, a saturation flash was applied and the effective quantum yield \(({\Delta}F/F{^\prime}_{\mathrm{m}})\) was determined at each light intensity step. From these data, the relative electron transport rate (rETR in μmol electrons m−2 s−1) was calculated as \(rETR{=}PPFD{\times}{\Delta}F/F{^\prime}_{\mathrm{m}}{\times}0.5.\) The obtained data were fitted to a model developed by Eilers and Peeters (1988) using the software KyPlot 2.0. The parameters α (the initial slope of the unsaturated curve, as ETR/PPFD), rETRmax (maximum rate of electron transport), and Ik (light saturation parameter, as rETRmax×α−1) were derived from these curves. Diurnal patterns of photosynthetic activity of C. glomerata and Vaucheria sp. were monitored on two clear days (1 June 1999 and 29 July 1999). Algal samples taken from HL and LL habitats were exposed at an HL site in the streambed. Once per hour \({\Delta}F/F{^\prime}_{\mathrm{m}}\) was measured in situ in each sample under natural sunlight. Subsequently, Fv/Fm was determined after darkening the sample for 5 min and applying far-red light for 20 s. Photodiodes (BPW-21, Centronics, GB), calibrated against sunlight with a Li-192 SA-sensor (Li-Cor, Lincoln, NE, USA), were used to record incident PPFD over the course of the day. Pigment analysis Samples for pigment analysis were taken on the same dates as samples for the P−I curves. Algal tufts were dry-blotted for 20 s between four layers of filter paper and then immediately frozen in liquid nitrogen. In the laboratory, pigment analysis was performed by HPLC as described by Ensminger et al. (2000) using a modified method of Büch et al. (1994). The HPLC system was calibrated using standards from Roche (Basel, Switzerland), and Sigma (St Louis, MO, USA). The algae examined belong to different divisions and thus show characteristic differences in their pigment compositions: C. glomerata (Chlorophyta) contains the chlorophylls a and b (Chl a and Chl b), and a photoprotective xanthophyll cycle, which converts violaxanthin (V) into the intermediate form antheraxanthin (A) and finally zeaxanthin (Z) during periods of high-light stress, whereas Vaucheria sp. (Heterokontophyta) contains the chlorophylls a and c (Chl c) and a xanthophyll cycle that converts diadinoxanthin (Ddx) directly into diatoxanthin (Dtx) upon exposure to high light. For statistical analysis, for C. glomerata, the ratio of Chl a:Chl b (Chl a/b) was used and the pool of the xanthophyll-cycle pigments per Chl a (VAZ/Chl a). Analogously, for samples of Vaucheria sp., the ratio of Chl a:c (Chl a/c) and the sum of Ddx and Dtx per Chl a ((Ddx+Dtx)/Chl a) were used. Statistics The patterns of vegetation obtained at 1 m distances along the transects were mapped and then correlated with measured abiotic variables by means of Canonical Correspondence Analysis (CCA; ter Braak, 1986) after a preliminary detrended correspondence analysis (DCA) showed a sufficient length of gradient value. The significance of the obtained CCA model was assessed by Monte Carlo tests (199 permutations). Running an additional CCA with a manual selection of the environmental variables allowed the relative importance of each variable to be calculated. Multivariate statistics were done using the software program Canoco 4.0 for Windows including CanoDraw and CanoPost. Parameters obtained from P−I curves and pigment analysis were compared by one-way ANOVA to test for significant differences between HL and LL habitats. Spearman's rank correlation was used to identify the relation of incident PPFD and physiological parameters of the algae. For this purpose the ‘light history’ was obtained by calculating the average daily sum of irradiance over a period of 10 d prior to the respective measurements, as this is a typical time-scale necessary to manifest acclimational changes in the composition of chlorophylls in Cladophora glomerata (I Ensminger, unpublished data). For samples from the experimentally shaded channels, the effective attenuation of PPFD by the nylon mesh shading (20% and 40%) of solar irradiance was taken into account. For samples taken from the naturally shaded habitats, an attenuation of 40% was assumed. For all statistics other than the correspondence analysis, the software package SPSS 9.0 (SPSS, Illinois, USA) was used. Results Abiotic factors Seasonal changes of abiotic factors are given in Fig. 1. The average daily discharge rate was above 5 m3 s−1 at the end of April. Except for the flooding event between 20 May and 23 May, discharge rates then constantly decreased to less than 1 m3 s−1 by the first week of July (Fig. 1A), followed by two distinct flooding events between 6 July and about 20 July. Light conditions were highly variable from late April to August, as indicated by the 3 d running average of the integrated radiation (Fig. 1B). Periods of moderate to high solar radiation were followed by low radiation periods, for example, the high levels of radiation during the middle of June were followed by the short low-energy period around 6 July. However, the effect of the expanding foliage of riparian vegetation effectively changed growth conditions within the studied transects (Fig. 1C). In late April the average level of radiation was typically between 90% and 75% at open and shaded sampling points, respectively. During summer and with the expansion of leaves by riparian vegetation, this difference between open and shaded sites increased, finally resulting in 90% (open) compared with 30% (at shaded sites). Water temperature at 12.00 h rapidly increased from about 5 °C in late April to typically 12–13 °C for most of May and June, except for a warm period at the start of June and later in July when temperatures were above 15 °C (Fig. 1D). Fig. 1. View largeDownload slide Seasonal changes in abiotic factors at the river Ilm. Average daily discharge rate (A); 3 d running average of the daily sum of radiance (B); relative levels of irradiance and their typical change within open and shaded sites; data points represent average values ±SD of 23 typically open and 18 transiently shaded sampling sites along the transects (C); water temperature at noon at the sampling sites, data points represent the average values of three measurements (with SD being smaller than the size of the symbols) (D). Arrow indicates the occurrence of summer flood. Fig. 1. View largeDownload slide Seasonal changes in abiotic factors at the river Ilm. Average daily discharge rate (A); 3 d running average of the daily sum of radiance (B); relative levels of irradiance and their typical change within open and shaded sites; data points represent average values ±SD of 23 typically open and 18 transiently shaded sampling sites along the transects (C); water temperature at noon at the sampling sites, data points represent the average values of three measurements (with SD being smaller than the size of the symbols) (D). Arrow indicates the occurrence of summer flood. Macroalgal distribution Seasonal patterns: Cladophora glomerata was the dominant algae in the studied stretch of the Ilm, followed by Audouinella hermannii Roth 1860 Duby, Hildenbrandia rivularis (Liebmann) J. Agardh, Vaucheria sp., and Stigeoclonium sp. For C. glomerata, Vaucheria sp., and Stigeoclonium sp., marked seasonal changes were observed during the transition from spring to summer (Fig. 2A). By contrast, other algae (e.g. A. hermannii) showed constant coverage values during the whole observation time (Fig. 2A). Maximum coverage of C. glomerata, with values between 25% and 29%, occurred between 8 May and 12 May and then suddenly decreased to about 10% by the end of the month, approximately 3 weeks before the summer flood occurred (Fig. 2A). This decrease in percentage cover was accompanied by decreasing maximum thallus length of C. glomerata (Fig. 2B) from more than 0.5 m in spring to less than 0.1 m in summer. However, median thallus length was within 0.05–0.1 m throughout the observation period. Fig. 2. View largeDownload slide Cumulative values of the observed benthic macroalgae coverage from 2772 observations normalized to the total area sampled (for species with coverage values <2% the inserted figure shows the same data on a smaller scale) (A), and the maximum (broken line) and median (dotted line) length of thalli of C. glomerata (B). Arrow indicates occurrence of summer flood. Fig. 2. View largeDownload slide Cumulative values of the observed benthic macroalgae coverage from 2772 observations normalized to the total area sampled (for species with coverage values <2% the inserted figure shows the same data on a smaller scale) (A), and the maximum (broken line) and median (dotted line) length of thalli of C. glomerata (B). Arrow indicates occurrence of summer flood. Environmental variables: Canonical correspondence analyses was used to detect correlations between the species distribution and the measured environmental variables (ter Braak, 1986). CCA directly relates data of community composition to the environmental variables, producing an ordination diagram in which the first axis spans the maximum variation of species distribution and thus has the highest explanatory value. The closer the environmental variables, represented by arrows, appear on the first or second axis, the higher their influence on the community. The arrows start from the origin of the diagram, which represents the grand mean of each environmental variable, and can be extended backwards. By dropping perpendiculars from each species point to the arrow of interest, a ranking of species with regard to the environmental variable can be obtained. The CCA of the dataset indicated that, at different times of the year, different sets of environmental factors affected the observed species distribution. A CCA based on the complete observation period from 20 April to 3 August was able to explain only 11.7% of the observed species distribution by environmental parameters (data not shown). Splitting the data into subsets of shorter time periods yielded much higher explanatory power and improved the relative importance of the measured abiotic factors. In spring (May), during the maximum coverage of C. glomerata, water depth and water current velocity were the most important factors (Fig. 3A). Together, both parameters explained 28.6% of the plotted species variance in the model. However, the statistical significance of this model was low. In the overall model the eigenvalue of the first axis was 0.126 and the environmental variables accounted for only 9.1% of the variance in species distribution. The second subset comprised two mapping events during the recolonization phase in summer (July/August), after a flooding event. Here, light intensity proved to be the most important parameter (Fig. 3B), accounting for 58.5% of the explainable variance in the species data. This shift in importance of environmental factors was accompanied by a general increase of explanatory values reached with the CCA procedure: in the second subset, the eigenvalue of the first axis reached 0.444, and the overall model explained 19% of the species variation with the environmental variables. Fig. 3. View largeDownload slide Canonical correspondence analysis (CCA) diagrams showing the correlation between the species distribution and environmental variables at two different times of the year. Spring subset (May 1999) (including the moss Fontinalis antipyretica L.) (A); and summer subset (July/August 1999) (B). All axes are significant (P >0.01; Monte Carlo Simulation, 199 permutations). The eigenvalue of the first axis is 0.126 for the spring subset and 0.444 for the summer subset. For further explanation, see text. Fig. 3. View largeDownload slide Canonical correspondence analysis (CCA) diagrams showing the correlation between the species distribution and environmental variables at two different times of the year. Spring subset (May 1999) (including the moss Fontinalis antipyretica L.) (A); and summer subset (July/August 1999) (B). All axes are significant (P >0.01; Monte Carlo Simulation, 199 permutations). The eigenvalue of the first axis is 0.126 for the spring subset and 0.444 for the summer subset. For further explanation, see text. In both subsets, C. glomerata was depicted close to the origin and grand mean of the important environmental factors. Thus, the average distribution of C. glomerata did not show any clear preference regarding the measured parameters but, rather, suggests that distribution was controlled by the average of these abiotic factors. This, in turn, reflects the ability of Cladophora to grow within a broad range of the abiotic factors. A similar distribution was found for Vaucheria sp. during the spring subset, when the CCA model indicated a preference for sites which are slightly less deep and have slightly lower current velocity. Since this alga was not present during the summer, it did not appear in Fig. 3B. Audouinella sp. was found at greater depths and higher velocities than was C. glomerata and Vaucheria sp. (Fig. 3A, spring subset). Stigeoclonium sp. and the diatoms preferred open habitats, whereas H. rivularis and Audouinella sp. were found more often in shaded habitats (Fig. 3B). According to the CCA analysis, C. glomerata was found in open as well as in shaded habitats but preferred higher light intensities. Preferences of C. glomerata and Vaucheria sp.: Presence–absence data of C. glomerata and Vaucheria sp. at the sampling sites were used to detect preferences for light conditions, depth of growth, water current velocity, and substrate size (Fig. 4). Over the total observation period, C. glomerata and Vaucheria sp. clearly favoured the open (high-light) sites (Fig. 4A), and the preferred water depth was 20 cm for Cladophora and 30–40 cm for Vaucheria (Fig. 4B). Neither of the two species occurred in deep water. This probably reflects the requirement of higher light intensities or a preference for fast-flowing water, as indicated in Fig. 4C; Cladophora and Vaucheria occurred most often at water current velocities of 20–30 cm s−1. The preference for fast-flowing water conditions is probably also reflected in the preferred substratum size (Fig. 4D). Both species were most present in substrate size class 4 and avoided areas where there were small stones and pebbles. Fig. 4. View largeDownload slide Preference of environmental conditions, indicated by the relative occurrence of Cladophora glomerata and Vaucheria sp. at the sampling points along the 20 transects during the period (April 1999 to August 1999). Light conditions in the five estimated classes (1=completely shaded, 2=shaded through most of the day, 3=received sunlight for about half of the day, 4=mostly open/received sunlight during most of the day, 5=completely open) (A); water depth (B); current velocity (C); and substrate size (1=sand, 2=small gravel, 3=medium-sized gravel, 4=coarse gravel, 5=stones, 6=boulders) (D). Closed bars, distribution of environmental conditions at all sites; shaded bars, environmental conditions at sites with occurrences of C. glomerata, open bars, growth conditions at sites with an occurrence of Vaucheria sp. Fig. 4. View largeDownload slide Preference of environmental conditions, indicated by the relative occurrence of Cladophora glomerata and Vaucheria sp. at the sampling points along the 20 transects during the period (April 1999 to August 1999). Light conditions in the five estimated classes (1=completely shaded, 2=shaded through most of the day, 3=received sunlight for about half of the day, 4=mostly open/received sunlight during most of the day, 5=completely open) (A); water depth (B); current velocity (C); and substrate size (1=sand, 2=small gravel, 3=medium-sized gravel, 4=coarse gravel, 5=stones, 6=boulders) (D). Closed bars, distribution of environmental conditions at all sites; shaded bars, environmental conditions at sites with occurrences of C. glomerata, open bars, growth conditions at sites with an occurrence of Vaucheria sp. Photosynthetic activity of C. glomerata and Vaucheria sp. Mean values and standard errors for the parameters α, rETRmax and Ik derived from the P−I curves are shown in Table 1. Samples of C. glomerata from HL habitats reached significantly higher rETRmax- and Ik-values than did samples from LL habitats, whereas the values for α did not differ among samples taken from different habitats. Bivariate correlations (Table 2) revealed a significant positive relationship of rETRmax and Ik-values to the light history of the C. glomerata samples (0.667 and 0.625, respectively; P <0.01, Spearman's rank correlation coefficient). Vaucheria sp. reached about the same levels of rETRmax as C. glomerata from LL habitats. Samples of Vaucheria sp. from different habitats did not differ in the measured parameters and did not reveal any correlation with the light history (Table 2). Diurnal measurements of the photosynthetic activity not only confirmed the results obtained from the light-response curves but also suggested different strategies of light utilization in both species. The optimum quantum yield of the dark-adapted sample (Fv/Fm) decreased in C. glomerata and in Vaucheria from morning to noon during times of high-incident PPFD and recovered completely by the evening when PPFD had decreased (Fig. 5A). However, Vaucheria sp. always retained relatively higher levels of Fv/Fm during the day (Fig. 5A). Effective quantum yield of the algae in the light \(({\Delta}F/F{^\prime}_{\mathrm{m}})\) revealed extremely low values for Vaucheria sp. at moderate light intensities of about 400 μmol m−2 s−1 (Fig. 5B) in contrast to C. glomerata, which maintained higher levels of \({\Delta}F/F{^\prime}_{\mathrm{m}}\) throughout the day. Interestingly, at 07.00 h and a PPFD of only 100 μmol m−2 s−1, \({\Delta}F/F{^\prime}_{\mathrm{m}}\) was already more than 30% lower in Vaucheria than in C. glomerata. The generally lower \({\Delta}F/F{^\prime}_{\mathrm{m}}\) in Vaucheria sp. suggests that a higher fraction of energy absorbed by photosystem II (PSII) does not undergo efficient photochemical energy conversion in PSII. This is illustrated in Fig. 5C, which shows the relative electron transport rate derived from measurements of chlorophyll fluorescence in C. glomerata to be generally higher than in Vaucheria sp., irrespective of the level of PPFD. Fig. 5. View largeDownload slide Different dynamics in photosynthetic activity of C. glomerata (n=3 ±SD) and Vaucheria sp. (n=2 ±SD) during a diurnal course (1 June 1999). Optimum quantum yield (Fv/Fm) (A); effective quantum yield in the light \(({\Delta}F/F{^\prime}_{\mathrm{m}})\) (B); and relative rate of electron transport (C). Open symbols, Vaucheria sp., closed symbols, C. glomerata: Incident photosynthetic photon flux density (PPFD) between 07.00 h and 18.30 h is given as a thin solid line in the background. Fig. 5. View largeDownload slide Different dynamics in photosynthetic activity of C. glomerata (n=3 ±SD) and Vaucheria sp. (n=2 ±SD) during a diurnal course (1 June 1999). Optimum quantum yield (Fv/Fm) (A); effective quantum yield in the light \(({\Delta}F/F{^\prime}_{\mathrm{m}})\) (B); and relative rate of electron transport (C). Open symbols, Vaucheria sp., closed symbols, C. glomerata: Incident photosynthetic photon flux density (PPFD) between 07.00 h and 18.30 h is given as a thin solid line in the background. Table 1. Photosynthetic performance of C. glomerata and Vaucheria sp. from different light habitats   Habitat   N   α (μmol electrons × μmol photons−1)   rETRmax (μmol electrons m−2 s−1)   Ik (μmol photons m−2 s−1)   Cladophora glomerata  HL  9  0.297±0.024  40.723±6.22**  134.616±12.98**    LL (40% of HL)  11  0.279±0.015  18.769±0.709**  69.336±5.058**  Vaucheria sp.  HL  15  0.203±0.018  18.799±1.660  113.900±21.950    LL (40% of HL)  10  0.181±0.021  20.268±1.659  120.164±13.095    LL (20% of HL)   5   0.221±0.038   17.720±3.061   88.655±15.594     Habitat   N   α (μmol electrons × μmol photons−1)   rETRmax (μmol electrons m−2 s−1)   Ik (μmol photons m−2 s−1)   Cladophora glomerata  HL  9  0.297±0.024  40.723±6.22**  134.616±12.98**    LL (40% of HL)  11  0.279±0.015  18.769±0.709**  69.336±5.058**  Vaucheria sp.  HL  15  0.203±0.018  18.799±1.660  113.900±21.950    LL (40% of HL)  10  0.181±0.021  20.268±1.659  120.164±13.095    LL (20% of HL)   5   0.221±0.038   17.720±3.061   88.655±15.594   Parameters were derived from P−I curves. N, number of samples; α, the initial slope of the P−I curve; rETRmax, maximum relative electron transport rate; Ik, light saturation parameters. All values are given ± the standard error of the mean. Significant differences between the samples from different habitats (HL, high-light habitats, and LL, low-light habitats) as detected by one-way ANOVA are indicated as follows: ** significant at the 0.01 level; * significant at the 0.05 level. View Large Table 2. Spearman's rank correlation coefficients for the correlations between the parameters α, rETRmax, and Ik as given in Table 1 and the light history comprising 10 d prior to each measurement   N   α (μmol electrons × μmol photons−1)   rETRmax (μmol electrons m−2 s−1)   Ik (μmol photons m−2 s−1)   Light history of C. glomerata  20  −0.176  0.670**  0.619**  Light history of Vaucheria sp.   30   −1.49   0.136   0.083     N   α (μmol electrons × μmol photons−1)   rETRmax (μmol electrons m−2 s−1)   Ik (μmol photons m−2 s−1)   Light history of C. glomerata  20  −0.176  0.670**  0.619**  Light history of Vaucheria sp.   30   −1.49   0.136   0.083   Significant correlations are indicated as follows: ** significant at the 0.01 level. View Large Photosynthetic pigments The results obtained from the pigment analysis for samples of C. glomerata and Vaucheria sp. are shown in Table 3 and Table 4, respectively. Samples of C. glomerata from HL habitats showed higher ratios of Chl a/b and contained more VAZ/Chl a compared to samples from LL habitats (Table 3). The light history of these samples from different habitats correlated significantly with the ratio of Chl a/b and resulted in a Spearman's rank correlation of 0.530 (P <0.01); the correlation with the ratio of VAZ/Chl a resulted in a value of 0.425 (P <0.01), respectively. In contrast to the light-induced acclimation of C. glomerata, samples of Vaucheria sp. from different habitats did not differ statistically significantly in pigment content or composition (Table 4). Table 3. Photosynthetic pigments of C. glomerata taken from HL and LL habitats Habitat   N   Chl a/b (mol mol−1)   VAZ/Chl a (mol mol−1)   HL  20  1.80±0.05**  0.16±0.01**  LL (40% of HL)   16   1.52±0.05**   0.13±0.01**   Habitat   N   Chl a/b (mol mol−1)   VAZ/Chl a (mol mol−1)   HL  20  1.80±0.05**  0.16±0.01**  LL (40% of HL)   16   1.52±0.05**   0.13±0.01**   The number of samples (N) and the mean ±SE are provided for the following parameters: Chl a/b, ratio of Chl a per Chl b; VAZ/Chl a, total xanthophyll-cycle pigments (violaxanthin+antheraxanthin+zeaxanthin) per Chl a. Significant differences between the samples from different habitats as detected by one-way ANOVA are indicated as in Table 1. View Large Table 4. Photosynthetic pigments of Vaucheria sp. taken from HL and LL habitats Habitat   N   Chl a/c (mol mol−1)   (Ddx+Dtx)/Chl a (normalized)   HL  17  27.11±1.42  0.87±0.05  LL (40% of HL)  7  24.20±2.08  0.79±0.12  LL (20% of HL)   7   30.66±4.17   1.11±0.11   Habitat   N   Chl a/c (mol mol−1)   (Ddx+Dtx)/Chl a (normalized)   HL  17  27.11±1.42  0.87±0.05  LL (40% of HL)  7  24.20±2.08  0.79±0.12  LL (20% of HL)   7   30.66±4.17   1.11±0.11   The number of samples (N) and the mean ±SE are provided for the following parameters: Chl a/c, ratio of Chl a per Chl c; (Ddx+Dtx)/Chl a, total xanthophylls of Ddx–xanthophyll cycle (diadinoxanthin+diatoxanthin) per Chl a (peak area of the accessory pigments normalized to the peak area of chl a). Significant differences between the samples from different habitats as detected by one-way ANOVA are indicated as in Table 1. View Large Discussion Macroalgal distribution Apparently the algal coverage changed markedly during the season, but no single species was as dominant as Cladophora glomerata at any time (Fig. 2A). Most striking was the pronounced decrease in coverage of C. glomerata, which was already visible in May, well before the summer flood events (Fig. 1A). Biotic factors such as control by grazers (Dodds and Gudder, 1992; Evans-White et al., 2001) or ageing (Dudley et al., 1986; Schönborn, 1996, see below) might account for this sudden decrease in the early summer population of C. glomerata, but overgrowth and shading/competition by epiphytes (Dodds, 1991) can be excluded from this analysis. The fraction of Chl c from the total content of chlorophylls in these samples, which can be used as a proxy for changes in the abundance of diatoms growing on Cladophora, was constant throughout the whole sampling period and was typically low, accounting only for about 2% of the total chlorophyll within Cladophora samples. Nonetheless, low discharge rates, prevalent in early summer (June) with reduced water velocities, are also disadvantagous abiotic factors for C. glomerata, which prefers moving waters (Whitton, 1970; Dodds, 1991). Schönborn (1996) stated that optimum water current velocities for C. glomerata are between 0.5 and 0.8 m s−1. The positive effect of increased water velocities is the improved acquisition of resources (Raven, 1992). Because warmer water carries fewer dissolved gases while organisms show increased metabolic rates, any negative effect of slow-moving water velocity would be additionally aggravated by the increased water temperature, leading to an even more unfavourable situation for C. glomerata. Similarly, Whitton (1970) described a period of maximum growth of C. glomerata in early summer followed by a rapid decline, and attributed the decrease to diminished levels of dissolved oxygen. However, it was also suggested that endogenous processes are responsible for the typical summer decline in biomass (Dudley et al., 1986; Schönborn, 1996); therefore the concomitant decrease in coverage and thallus length could also be due to fragmentation of the thallus (Fig. 2B). Important abiotic factors Over the course of the observation period, different combinations of the measured abiotic environmental variables explained the observed distribution of the benthic algae. In the spring, water depth and water velocity accounted for most of the species distribution (Fig. 3A), but over time the importance of light intensity increased. In the end, light proved to be the most powerful environmental variable (Fig. 3A). At the same time, the explanatory power of the CCA model increased, reaching an eigenvalue of >0.4. The shift in the relative importance of the measured environmental variables reflects the change of growth light conditions at the sampling points (Fig. 1C). During early spring all sites received equal quantities of light, but eventually the increasing foliage of the riparian vegetation transiently altered the light conditions, creating shaded and open habitats. Thus macroalgal distribution was most affected during summer. Vaucheria sp. seems to have been most drastically affected by this seasonal change in growth light conditions. This species had a tendency to occur at non-shaded sampling points and at a moderate water depth, typically in the range 30–40 cm, which still allows light to penetrate the water column (Fig. 4A, B). In spring, Vaucheria sp. relied on the same kind and similar magnitude of abiotic factors as C. glomerata (Figs 3A, 4), but then it completely disappeared from the stretches investigated during the summer (Figs 1A, 3B, 4). Cladophora glomerata remained the dominant alga even under the altered environmental conditions. This suggests opportunistic behaviour on the part of C. glomerata in response to a range of abiotic factors (and thus a high capacity of plasticity), whereas Vaucheria sp. seems to be more restricted in its distribution. In this study it much preferred open unshaded sites. However, other species with a pronounced preference for certain growth light conditions, e.g. Stigeoclonium sp., which prefers open habitats (Hill, 1996) or H. rivularis, which prefers shaded habitats (Kremer, 1983), also occurred late in the season. These species, rather than Vaucheria sp., probably contributed to the higher explanatory power of the summer subset. The higher explanatory values of the CCA for the summer period are also attributed to a recolonization phase after the summer flood. Such disturbances are presumed to reset the ecosystem, after which abiotic factors become important; biotic interactions usually gain importance only after periods of relative stability (Townsend, 1989). Species differences in photosynthetic light use These physiological measurements reveal two different strategies in photosynthetic light use in Vaucheria sp. and C. glomerata. \({\Delta}F/F{^\prime}_{\mathrm{m}}\) -values were consistently higher in C. glomerata than in Vaucheria sp. (Fig. 5B), resulting in higher rETR and twice as high rETRmax-values (Fig. 5C; Table 1). During a diurnal course at high-incident PPFD around noon, Fv/Fm-values in C. glomerata substantially declined (Fig. 5A), typically indicating dynamic photoinhibition in plants (Osmond, 1994) and algae (Hanelt, 1998; Ensminger et al., 2001). At the same irradiance Vaucheria sp. retained considerably higher Fv/Fm. Interestingly, these increased Fv/Fm levels in Vaucheria sp. were associated with lower \({\Delta}F/F{^\prime}_{\mathrm{m}}\) -values than those observed in C. glomerata. The difference in the quantum yield of PSII of dark-adapted samples (Fv/Fm) versus the quantum yield of a light-adapted sample \(({\Delta}F/F{^\prime}_{\mathrm{m}})\) of Vaucheria sp., together with generally high values of Fv/Fm, clearly indicate that the photosystem was not impaired. Instead, Vaucheria sp. dissipates a greater fraction of absorbed energy non-photochemically. In higher plants and green algae (Chlorophyta) non-photochemical dissipation of excess energy is usually correlated with the reversible conversion of violaxanthin via antheraxanthin into zeaxanthin (VAZ cycle; Demmig-Adams and Adams, 1992; Horton et al., 1994; Olaizola and Yamamoto, 1994). In xanthophyte algae like Vaucheria sp., the Ddx/Dtx cycle represents this light-protecting mechanism. The de-epoxidation of this system in the light operates considerably faster than does the VAZ cycle (Olaizola and Yamamoto, 1994; Lohr and Wilhelm, 1999), explaining the quick decrease in \({\Delta}F/F{^\prime}_{\mathrm{m}}\) once Vaucheria was exposed to about 200 μmol photons m−2 s−1 (Fig. 5B). While the de-epoxidation step is quick for many organisms with the Ddx/Dtx cycle (Casper-Lindley and Björkman, 1998), the epoxidation step is often much slower than is the case for organisms with the VAZ cycle (Kashino and Kudoh, 2003). This contradicts the fast recovery of the measured chlorophyll fluorescence parameters in Vaucheria sp. (Fig. 5A, B). Within only 5 min of recovery in the dark, levels of Vaucheria sp. went from extremely low to much higher levels of Fv/Fm than those observed in C. glomerata. This suggests that the involvement of additional quenching processes in the light-harvesting antenna, for example, reaction centre quenching, may be contributing to the quick recovery of the fluorescence parameters (Olaizola and Yamamoto, 1994). Phenotypic plasticity, such as the ability of an organism to acclimate photosynthetically to different light intensities, is reflected through the differences in photosynthetic performance or photosynthetic pigments of individuals from different habitats: Organisms adapted to high-light conditions reach higher maximum photosynthetic or electron transport rate at high-light intensities, whereas shade-adapted organisms usually use low light more efficiently, as indicated by higher values of α (Boston and Hill, 1991; Osmond, 1994; Hill, 1996; Walters, 2005). In this study's experiments C. glomerata dynamically acclimated to different light intensities. HL-grown samples displayed higher rETRmax and Ik-values than did samples from LL habitats, which is consistent with earlier data from C. glomerata (Ensminger et al., 2000, 2001). The difference between HL and LL was attributed to the previous 10 d of light history, which was significantly positively correlated with rETRmax- and Ik-values. However, α did not show any significant differences between samples taken from different habitats, and there was no correlation with the light history. While the regulation of α may be controlled as well by other environmental clues, it is suggested that acclimational changes in α might not be detectable with the chlorophyll-fluorescence technique used here and from the rates of electron transport between PSII and PSI. For example, Silva et al. (1998) used chlorophyll fluorescence in a similar way to test the acclimation to different light intensities in the marine red alga Gelidium sesquipedale. They also found that HL samples (from shallow water) reached higher values for rETRmax and Ik compared with LL samples (from deeper waters), but they did not find any significant differences in α. In general, one would expect a decrease in α as a result of an imbalance between energy absorbed by the light-harvesting systems and the energy consumed by Calvin-cycle reactions. Simply put, chlorophyll fluorescence as a probe for PSII and its activity might remain unaffected to some extent by limitations in Calvin-cycle activity at high-light intensities, as long as alternative electron sinks are able to maintain an electron flow from PSII. Such photoprotective alternative sinks for electrons are realized by the water–water cycle (Asada, 2000), photorespiratory processes, or cyclic electron flow around PSI (Ensminger et al., 2001; Munekaga et al., 2004). Additional evidence for the acclimation of C. glomerata to different growth light conditions was provided by the pigment data. Samples from HL habitats reached higher ratios of Chl a/b, suggesting a lower amount of antenna chlorophylls per reaction centre; in addition, they contained more VAZ/Chl a (Table 3), indicating increased excitation pressure and therefore higher capacity for harmless dissipation of excess light via non-photochemical quenching and the xanthophyll cycle (Demmig-Adams and Adams, 1992; Brugnoli et al., 1998; Ensminger et al., 2001; Gevaert et al., 2003). By contrast, Vaucheria sp. did not acclimate to different light intensities in these experiments, neither on the level of pigments nor regarding photosynthetic light use. Even under deep-shade conditions (20% of the apparent PPFD), it was not possible to discern any difference that was induced by the light conditions of the different treatments. In the stream it was observed that Vaucheria sp. most often grows under HL conditions and particularly well in the open flow-through channels under experimental conditions. Because of this preference for open habitats in the experimental system of this study (see also Fig. 4A) and the low rETR-values, together with the relatively high values of Ik compared with the observed Ik-values in HL C. glomerata, it is suggested that Vaucheria sp. represents a different strategy of light exploitation. Vaucheria sp. appears only in open HL conditions where it constitutively quenches a large fraction of the absorbed light through the rapid diadino/diatoxanthin cycle non-photochemically, whereas C. glomerata represents an opportunistic euryoecious species, which is able to modify its photosynthetic performance in response to the prevailing light conditions. Photosynthesis linked to small-scale distribution patterns Both CCA models depicted C. glomerata very close to the origin in Fig. 3, suggesting a preference of C. glomerata near the grand mean of the measured environmental factors. Alternatively, this might also indicate euryoecious traits in C. glomerata, as this species can grow within the wide range of environmental factors that this analysis depicted; thus the centre of its distribution is similar to the grand mean of the environmental factors. It is not possible to distinguish between these two possibilities by using only the multivariate statistics used here. However, the ecophysiological experiments clearly revealed the acclimation of C. glomerata to the growth light conditions, indicating a euryoecious response to this abiotic factor. Acclimation to growth light conditions provides effective energy conversion and enhances the probability of survival for C. glomerata. Vaucheria sp. was favoured by high-light conditions, as shown by its fast xanthophyll cycle and subsequently decreased level of photoinhibition. But less efficient energy conversion can contribute to limited growth and distribution, especially under low-light conditions (shaded habitats). In addition, development and maintenance of protective mechanisms are attributed to energy costs (Long et al., 1994), possibly another factor that reduces growth. In conclusion, the capacity to acclimate photosynthesis was more pronounced in a species that was found growing in both exposed and shaded environments, thus confirming patterns also observed in higher plants (Murchie and Horton, 1997). Under changing environmental conditions, which are typical for many freshwater streams, phenotypic plasticity is beneficial for the dominance and fitness of a species. Clearly, plants and algae with strong acclimation are more likely to succeed (Walters, 2005). This physiological plasticity is the great advantage of C. glomerata over other macroalgae, for example, Vaucheria sp. Both algae can occupy open habitats where they have to cope with high levels of solar irradiance during the day, but only C. glomerata is able to adjust photosynthesis to decreasing growth light conditions due to expanding riparian foliage in the early summer. However, since larger amounts of Vaucheria sp. were found at other sites along the Ilm, additional limiting factors, such as biotic interactions during relative stability, must be relevant as well. Nonetheless, there is increasing understanding of the coupling of physiological plasticity and species distribution not only in trees (Tognetti et al., 1997; Valladares et al., 2002) but also in corals (Anthony and Hoegh-Guldberg, 2003), seagrasses (Durako et al., 2003), and marine macroalgae (Raniello et al., 2004) that corroborates these results on freshwater macroalgae. 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TI - Plasticity and acclimation to light reflected in temporal and spatial changes of small-scale macroalgal distribution in a stream
JF - Journal of Experimental Botany
DO - 10.1093/jxb/eri203
DA - 2005-07-04
UR - https://www.deepdyve.com/lp/oxford-university-press/plasticity-and-acclimation-to-light-reflected-in-temporal-and-spatial-SpGGcm7IfI
SP - 2047
EP - 2058
VL - 56
IS - 418
DP - DeepDyve
ER -