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Regulation of submersed macrophyte biomass in a temperate lowland river: Interactions between shading by bank vegetation, epiphyton and water turbidity
Aquatic Botany 92 (2010) 129–136
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Regulation of submersed macrophyte biomass in a temperate lowland river: Interactions between shading by bank vegetation, epiphyton and water turbidity Jan Ko¨hler *, Justyna Hachoł 1, Sabine Hilt Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mu¨ggelseedamm 301, 12587 Berlin, Germany
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 June 2009 Received in revised form 21 October 2009 Accepted 30 October 2009 Available online 5 November 2009
Growth of aquatic vegetation is often controlled by light supply, which is potentially decreased by bank vegetation, water turbidity and epiphytic biofilm. To understand the relative importance of these shading factors and the interactions between them we analysed the seasonal course of macrophyte biomass, shading by bank vegetation, turbidity of the water column and epiphytic light absorption in shaded and sunny sections of a temperate eutrophic lowland river. At a shaded site, bank vegetation decreased the light supply by 79%, 0.5 m water column by 45% and 2-week-old epiphyton by 28% during the vegetation period. Growth of submersed macrophytes, but not of epiphyton, was light-limited in the shaded sections. We found a saturation-type correlation between light supply and macrophyte biomass. Therefore, the additional light absorption of the water column or epiphyton only shortened the period of optimum light supply at the sunny site, but was crucial for macrophyte development at the shaded site. Light absorption of phytoplankton was most important in spring and that of epiphyton in late summer. Submersed macrophytes effectively retained particles and thus improved light supply of downstream stands, but this positive feedback effect was only relevant for shaded sections in summer. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Aquatic vegetation Growth Light absorption Light limitation Microphytobenthos Phytoplankton retention
1. Introduction Macrophytes are a key component of aquatic communities in many streams and lowland rivers. Long-term (Sand-Jensen et al., 2000) as well as spatial changes (Vannote et al., 1980) in biomass and composition of aquatic vegetation are often caused by changes in light supply. In general, three different external factors control light supply of submersed macrophytes in rivers: shading by bank vegetation (Dawson and Kern-Hansen, 1979; Wright et al., 1982; Davies-Colley and Quinn, 1998), light absorption in the water column by suspended algae, mineral particles and dissolved coloured substances (Hudon et al., 2000) and light absorption of the epiphytic biofilm (Chambers and Kalff, 1985; Asaeda et al., 2004). These factors have usually been analysed separately; few studies have dealt with combined effects of water turbidity and epiphyton (e.g., Sand-Jensen and Søndergaard, 1981; Vermaat and De Bruyne, 1993). However, the single attenuation components are not independent and interact in different ways. Shading by bank vegetation may not only limit growth of submersed macrophytes but also that
* Corresponding author. Tel.: +49 30 64181687; fax: +49 30 64181682. E-mail addresses: [email protected] (J. Ko¨hler), [email protected] (J. Hachoł), [email protected] (S. Hilt). 1 Present address: Institute of Environmental Development and Protection, University of Environmental and Life Sciences, Pl. Grunwaldzki 24, 50-363 Wroclaw, Poland. 0304-3770/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2009.10.018
of epiphyton (e.g., Hill et al., 2001), potentially resulting in an inverse relation between shading by trees and light absorption by epiphyton. Phytoplankton shades both epiphyton and submersed macrophytes, which potentially counterbalances the overall effect of phytoplankton shading. In addition, concentrations of phytoplankton and other suspended particles often decline during passage of macrophyte stands (e.g., Schulz et al., 2003a; Quinn et al., 2007). Therefore, density of macrophyte stands and light attenuation of the water column are potentially inversely related. This positive feedback could support growth of submersed macrophytes at downstream sites but might be compensated by higher epiphyton biomass if epiphyton growth is light-limited. All these effects are subject to distinct seasonal changes. Additionally, the importance of shading effects on macrophyte growth depends on the relation between growth and light supply. A linear relation, as was found by Dawson and Kern-Hansen (1979) and Sand-Jensen et al. (1989), would imply a similar relative decline in growth rate by any additional shading. In the case of a saturation-type relation between light and growth (e.g., Vermaat and Verhagen, 1996), however, additional shading would have no effect at saturating light intensities, but could be crucial at light limitation. Here, we compared annual courses of light supply and development of submersed macrophytes, epiphyton and phytoplankton at a sunny and a shaded site as well as maximum macrophyte biomass at 28 transects of different shading grade in a eutrophic, medium-sized, temperate lowland river to test the following hypotheses:
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(1) The relation between biomass of submersed macrophytes and light supply is non-linear, i.e. effects of additional shading depend on present light intensity. (2) Growth of submersed macrophytes in medium-sized lowland rivers is mainly influenced by shading from bank vegetation; shading by phytoplankton and epiphyton may additionally limit growth at certain times and water depths. (3) The shading effect of bank vegetation on submersed macrophytes is partly compensated by lower biomass and thus less shading of (light-limited) epiphyton. (4) Submersed macrophytes improve their own light supply by retaining suspended particles, but this positive feedback is also partly compensated by higher epiphyton biomass. 2. Methods 2.1. Study site The Spree is a eutrophic lowland river in North-Eastern Germany. It originates in the Lusatian Mountains (Saxony) and flows for 380 km through several reservoirs and shallow lakes to Berlin. There, the River Spree merges with the Havel, a tributary of the Elbe river (detailed description in Ko¨hler and Hoeg, 2000). The lower part of the Spree system, where this study was carried out, follows a former glacial spillway. The channel has a mean slope of about 0.13% and a width between 20 and 50 m. At mean discharge, 73% of the river course (river-km 302–334) is deeper than 1.0 m, 39% deeper than 1.5 m, and 9% deeper than 2.0 m. The river water level is measured daily by the Waterways and Shipping Administration Berlin (km 302) and by the State Department of Environment Brandenburg (km 328). These authorities estimated daily discharge from regularly updated stage–discharge relationships. Depths and volume of the water body were calculated from about 300 cross-section profiles of water depth and the daily water levels. The mean flow velocity was estimated from the volume of the water body, rate of discharge and length of the river stretch between the gauges. We conducted measurements at one shaded and two sunny transects of the River Spree. At the shaded site both banks were densely lined with trees (mainly black alder (Alnus glutinosa (L.) Gaertn.) and poplar (Populus canescens (Aiton) SM.), whereas only some trees were present on the northern bank of the sunny sites. 2.2. Macrophyte biomass Cover of the main species of submersed macrophytes was mapped monthly between May and October 2006 at a sunny (river-km 321) and a shaded (river-km 322) transect. Additionally, 28 transects covering a range of shading grades were mapped in July 2006. At each transect, a boat was moved between two ropes across the river to map a 6 m swath over the whole breadth of the river. Cover of each species was estimated visually in a grid of 1 m 2 m at three depths (bottom, middle and surface) using four classes: 0–10%, 10–40%, 40–70% and 70– 100%. The aboveground biomass of submersed macrophyte stands was harvested in July 2006 by diving using a 0.5 m 0.5 m metal frame. Macrophytes were separated into species, weighed and dried at 70 8C until weight constancy to determine dry weight (DW). Fresh weight (FW) of the harvested stands was correlated with the estimated cover and this speciesspecific ratio (biomass per relative cover) was used to calculate the fresh weight of each abundant species per m2 river bottom. In order to have at least ten replicates per species, the results of analogous harvests in 2001 (Schulz et al., 2003b) and in 2005 (J. Ko¨hler, Unpublished data) were included in the calculation of biomass per cover ratios.
2.3. Epiphyton biomass Epiphyton biomass was measured on artificial substrate exposed at a shaded site (km 322) and at a sunny site (km 315). Exposure was started on 26 April 2006, and epiphyton samples were collected fortnightly from 10 May to 11 October 2006. Epiphyton grows on both old and fresh leaves of submersed plants so we measured its biomass after 2 weeks exposure in consecutively repeating intervals (hereafter called ‘‘2-week epiphyton’’) as well as after 4–24 weeks exposure) from 26 April till the date of subsampling (hereafter called ‘‘total epiphyton’’). A similar approach was described in Vermaat and De Bruyne (1993). Artificial substrate consisted of transparent polypropylene sheets with a slightly textured surface (IBICO1, Germany). A4 (210 mm 297 mm) sheets were subdivided into ten strips held together like a comb. Substrates were placed in macrophyte-free areas and suspended 50 cm below the water surface. The sheets were fixed at the upstream side between small aluminium fillets and kept in horizontal position by the current. Every second week, four strips of the total epiphyton and the 2-week epiphyton series were sampled per site. Additionally, five pieces of Sagittaria sagittifolia L. (1.13 cm2 each) were collected at both river sites for pigment analyses at 15 August and 6 September 2006. Each substrate strip was slid into a separate damp plastic container, which was placed in a dark thermobox with some water at its bottom to provide 100% humidity during transport to the lab. Within hours of sample collection, the epiphyton was scrubbed from the substrate using a toothbrush, and suspended in a defined amount of GF/F-filtered river water. After homogenization, subsamples of each suspension were filtered onto three GF/F glass-fibre filters. One pre-weighed and pre-washed filter was dried at 105 8C to analyse dry weight and the contents of organic carbon and nitrogen as described below. One filter was frozen at 80 8C for later HPLC analysis and a third one used for absorption measurements. For pigment analyses, filters and plant pieces were freeze-dried and pigments were extracted by vibration shaking (2000 rpm, 1.5 h) with dimethylformamide and glass beads (0.75–1.0 mm diameter). After centrifugation for 20 min (2500 g, 4 8C), pigments were separated, identified and quantified with a HPLC system (Waters, USA) as described by Fietz and Nicklisch (2004). Fucoxanthin and chlorophyll b were used as marker pigments for diatoms and chlorophytes, respectively. Algae from other groups with the same marker pigments were not detected by microscopic analysis. We estimated the relative contributions of diatoms and chlorophytes to total epiphyton chl a by multiple linear regression (see, e.g., Fietz and Nicklisch, 2004): chl a ¼ 2:456 fucoxanthin þ 3:437 chlorophyll b R2 ¼ 0:99; p < 0:001:
(1)
The high coefficient of determination proofs a nearly constant ratio of marker pigment to chl a within the algal group. Epiphyton biomass was always related to the area of the artificial substrate. Immediately after filtration, the wet ‘‘absorption filter’’ was used to measure light absorption spectra (against blank wet filter) in a double-beam spectrophotometer (Shimadzu UV-VIS 2101). The mean optical density at 740–760 nm (OD740–760) was subtracted, filter effects were corrected according to Bricaud and Stramski (1990) and the absorption coefficient of the particles (a) was calculated as a ¼ ðODl OD740760 Þ
AF V S AS V F
(2)
where ODl is the optical density at a given wavelength, AF the clearance area of the filter, AS the area of the substrate strip, and VS
J. Ko¨hler et al. / Aquatic Botany 92 (2010) 129–136
and VF are the volumes of the epiphyton suspension per strip and of the filtered suspension, respectively. The percent light absorption (A) of epiphyton was calculated as A ¼ 100 ð1 10a Þ
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homogeneity of variance and log-transformed where necessary. Transformation satisfied the requirements in all cases. All analyses were carried out using the statistical package SPSS 14.0 (SPSS Inc., Chicago, IL).
(3) 3. Results
and averaged for 400–700 nm. 2.4. Light availability Global radiation was continuously recorded from a monitoring station at Lake Mu¨ggelsee, about 20 km downstream of the river sites. Photosynthetically available radiation (PAR) was calculated as 46% of net global radiation (=gross global radiation minus reflection and backscattering, see Baker and Frouin, 1987). The shading effect of riverbank vegetation was continuously recorded with a cosine-corrected PAR sensor (Li-Cor Biosciences, Lincoln, Nebraska) at the shaded exposure site. Underwater light extinction was calculated from light intensities simultaneously measured with spherical quantum sensors (Li-Cor Biosciences) in two water depths using the Lambert–Beer law. Light intensity at the 28 transects, where macrophytes were mapped in July, was calculated from measured intensities at the sunny and the shaded site and the canopy cover of bank trees estimated from aerial photographs. PAR attenuation by seston and epiphyton was interpolated between sampling dates. Interpolated attenuation data and continuously measured global radiation were used to calculate daily means of light availability at the water surface, for epiphyton growth in 0.5 m depth (net PAR multiplied by the percent light attenuated by the water layer) and for macrophytes (as above, then multiplied by percent light absorption of epiphyton). 2.5. Seston, nutrient availability, pH and water temperature Water samples were collected fortnightly at the beginning (river-km 302) and the end (km 332) of the river course, which did not receive any tributaries or wastewater inflows. The average value of both sites was used for our analyses. Water temperature and pH were measured immediately after sampling (pH probe, WTW, Weilheim, Germany). In the laboratory, two subsamples were filtered onto pre-washed and pre-weighed GF/F glass-fibre filters as described above, dried at 105 8C overnight and weighed to determine seston DW. Nitrogen (N) and carbon (C) content were determined using a Vario EL analyser (Elementar) after removing the carbonates by treatment with HCl. Each filter was wetted with some drops of 0.5 M HCl until no more foaming occurred and was allowed to dry overnight at 36 8C. Nutrient concentrations (total phosphorus: TP, soluble reactive phosphorus: SRP, total nitrogen: TN, dissolved inorganic nitrogen: DIN (=nitrate + ammonium), dissolved reactive silica: DSi, dissolved inorganic carbon: DIC), were measured using standard methods (Anonymous, 2005). Phytoplankton pigments were analysed in subsamples concentrated on GF/F filters as described for epiphyton pigments. 2.6. Statistical analyses Differences between the two river sites were tested by analyses of variance (ANOVA). We used a repeated measure ANOVA with time as the within-subjects factor and site as the between-subjects factor. Maximum biomass data of submersed macrophytes at 28 sites were compared using a one-way ANOVA and subsequent multiple comparisons with Tukey’s post hoc test at p < 0.05. Significance of changes in nutrient concentrations, discharge and water temperature between the exposure sites was tested by paired-samples t-tests at p < 0.05, assuming a linear change along the whole river course. All data were tested for normality and
3.1. Nutrient availability, pH, water temperature and hydrological conditions Concentrations of SRP during the investigated period averaged at 58 21 (standard deviation) mg L1 and fell below 50 mg L1 only in spring (April–early May). The mean concentration of DIN was 337 105 mg L1, values below 100 mg L1 were not found. The molar N:P ratio (DIN:SRP) fell below 16 (‘‘Redfield ratio’’) from June through early October, indicating a relative shortage in nitrogen. The concentrations of DSi and DIC were always higher than 2 and 20 mg L1, respectively. The pH averaged at 7.64 0.24. In epiphyton, the molar C:N ratios ranged between 5 and 7 in May and at the beginning of June and, in total epiphyton also in September–October (sun) and in October (shade). C:N ratios above 10 were only found in 2-week epiphyton (at August 15, sun, and in July, shade). In all other samples, C:N ratios ranged between 7 and 10. Monthly mean water temperature rose from 10.6 8C in April to 23.4 8C in July and declined to 14.0 8C in mid-October. The water discharge declined from April (15.6 1.7 m3 s1) to July–August 2006 (2.6 0.9 m3 s1). It increased again in September–October to 5.8 1.5 m3 s1. Due to the impounding effects of downstream lakes and dense stands of aquatic vegetation in the river, the mean depth of the river stretch was only slightly higher in April (1.42 0.04 m) than in July–August (1.22 0.08 m) and in September–October (1.30 0.06 m). Therefore, the mean velocity of flow paralleled the seasonal course of discharge. Monthly averages of flow velocity declined from 36 1 cm s1 in April to 8 2 cm s1 in July and August and increased again to 21 3 cm s1 in October 2006. On average, concentrations of TP and DSi as well as water temperature and discharge did not significantly change between sites. The mean concentrations of SRP (+11%) and of DIN (+7%) increased whereas TN declined (2%) from the sunny to the shaded site. 3.2. Light availability for epiphyton Net PAR (gross PAR minus albedo) averaged at 33.8 E m2 d1 (sunny site) and at 6.4 E m2 d1 (shade) at the water surface during the exposure period. Global radiation was reduced by cloudy periods mainly in the second half of May and in August but was 20–38% higher than the long-term average (1976–2005) in the first half of May, in June–July and September 2006. Bank vegetation reduced the mean light intensity at the shaded site by about 60%, at the beginning and the end of the exposure period, and by 83 4%, in July–August (Fig. 1). At the beginning of the river course, phytoplankton attained a maximum chl a in early May (88 mg L1) and a mean chl a of only 18 mg L1 in June–July. Seston DW was also highest in late spring (14.8 mg L1 at May 9) and lowest in June–July (5.3 0.4 mg L1). It increased again in late summer to autumn. Along the 30 km river section between km 302 and 332, phytoplankton chl a remained nearly constant in March–May but declined by 76 18% during passage in June–September. Accordingly, mean light attenuation in the water column declined from 1.45 0.17 to 1.04 0.12 m1 and mean light intensity in 0.5 m depth increased from 17.0 7.5 to 20.9 8.6 E m2 d1 along this river stretch (no shade by bank vegetation, average of June–September). On average of the whole river section, the mean coefficient of vertical light attenuation declined from 3.07 m1 (first half of May) to 1.07 m1 in June and
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Fig. 1. Light intensity (PAR) at the water surface (solid line), in 0.5 m depth (dotted line) and available for submersed macrophytes in 0.5 m depth covered by 2-week epiphyton (filled area) at the sunny (top) and the shaded site (bottom) of the Spree.
0.78 m1 in July–August and increased again to 1.27 m1 in September and 1.87 m1 in early October. During the exposure period, a 0.5 m water column attenuated on average 45 15% of the surface light intensity. The resulting PAR at a water depth of 0.5 m averaged at 18.7 E m2 d1 (sun) and 3.3 E m2 d1 (shade, Fig. 1, Table 1). 3.3. Development of epiphyton Total epiphyton grew continuously at the sunny site of the river from May until August, reaching a maximum of 33.4 g DW
per m2 artificial substrate. At the shaded site, total epiphyton grew rapidly in May and June to 17.2 g DW m2, declined in July and grew again for the remaining exposure time (Fig. 2a). Total epiphyton DW and total chl a were not significantly different between both sites. Diatom chl a was higher and chlorophyte chl a was lower at the shaded than at the sunny site (Table 2). Dry weight, total chl a and diatom chl a of 2-week epiphyton were significantly higher at the shaded than at the sunny site (Fig. 2a, Table 1). Chlorophyte chl a and the ratio of particulate organic C to N did not differ. The relative proportion of chl a to C content was slightly lower at the shaded site, compared to the sunny one (Table 1). Net growth rates of epiphyton were calculated as chl a increase per day after 2 weeks of exposure. Diatoms attained highest net growth rates at the sunny river site in the first half of June (2.2 mg chl a m2 d1) and at the shaded site at the end of June (1.2 mg chl a m2 d1). Maximum growth of chlorophytes was found 2 weeks later, but their accrual rates never exceeded 0.5 mg chl a m2 d1. Biomass of epiphytic diatoms was estimated from fucoxanthin concentrations of S. sagittifolia pieces at two sampling dates. Diatom chl a per m2 leaf area averaged at 36.9 14.6 mg (sun), 25.2 5.0 mg (shade, 15 August) and 8.0 1.4 mg (6 September 2006, sun). Diatom chl a did not significantly differ between plastic strip and leaf at the shaded site at 15 August (p = 0.38) and at the sunny site at 6 September (p = 0.18). A significantly (p = 0.045) lower diatom chl a was found on the artificial substrate compared to the leaf at the sunny site at 15 August (15.4 4.2 mg m2).
Table 1 Mean dry weight, chlorophyll a (chl a, both per m2 of artificial substrate) and chemical composition of 2-week epiphyton grown on artificial substrates at a sunny and a shaded site in the River Spree between 26 May and 11 October and of light availability (PAR: photosynthetically active radiation—at the water surface, for epiphyton and for macrophyte growth in 0.5 m depth) between 29 April and 11 October, analysed using a repeated measures ANOVA with site as between and time as within subjects. Parameter
Site 2
n
ANOVA
df
F
p
Sun Shade
3.5 3.5 5.1 3.4
10
Date Date site Site
9 9 1
12.8 10.1 41.3
<0.001 <0.001 0.001
Chl a total (mg m2)
Sun Shade
8.0 8.2 12.3 9.4
10
Date Date site Site
9 9 1
30.4 26.6 18.1
<0.001 <0.001 0.005
Diatom chl a (mg m2)
Sun Shade
6.2 6.5 10.6 8.4
10
Date Date site Site
9 9 1
24.7 25.2 22.7
<0.001 <0.001 0.003
Chlorophytes chl a (mg m2)
Sun Shade
1.8 2.1 1.8 1.7
10
Date Date site Site
9 9 1
51.9 19.9 0.01
<0.001 <0.001 0.97
C/N (molar)
Sun Shade
8.2 1.6 8.6 1.5
10
Date Date site Site
9 9 1
61.6 28.1 5.3
<0.001 <0.001 0.06
Chl a/C
Sun Shade
93 72 70 54
10
Date Date site Site
9 9 1
26.2 37.7 11.0
<0.001 <0.001 0.016
Light absorption by periphyton (%)
Sun Shade
22.3 14.2 33.0 14.1
10
Date Date site Site
9 9 1
39.1 12.1 115
<0.001 <0.001 <0.001
PAR at water surface (E m2 d1)
Sun Shade
33.8 14.2 6.4 2.6
11
Date Date site Site
10 10 1
20.4 11.9 931
<0.001 <0.001 <0.001
PAR for periphyton (E m2 d1)
Sun Shade
18.7 10.1 3.3 1.2
11
Date Date site Site
10 10 1
34.5 22.8 903
<0.001 <0.001 <0.001
PAR for macrophytes (E m2 d1)
Sun Shade
14.5 6.6 2.4 0.8
11
Date Date site Site
10 10 1
17.3 13.4 1035
<0.001 <0.001 <0.001
Dry weight (g m
)
Mean SD
J. Ko¨hler et al. / Aquatic Botany 92 (2010) 129–136
133
Fig. 3. Percent PAR absorption plotted against dry weight of epiphyton on artificial substrate exposed in 0.5 m water depth and fitted exponential curve (Eq. (4)).
3.4. Light available to submersed macrophytes Light absorption by total epiphyton increased during the first 2 months (Fig. 2b). Between 26 April and 11 October, total epiphyton reduced the incoming PAR by 61 17% at the sunny and by 71 15% at the shaded river site (Table 2). Two-week epiphyton absorbed 22 14% (sun) and 33 14% (shade) of the incoming PAR, respectively. Mean light absorption of both total and 2-week epiphyton was significantly higher at the shaded than at the sunny site (Tables 1 and 2). The percentage of absorbed light (A) and epiphyton DW were highly significantly correlated (p < 0.001; Fig. 3): A ¼ 100 ð1 e0:083DW Þ Fig. 2. Development of epiphyton and submersed macrophytes at a sunny (solid lines) and a shaded site (dotted lines) in the River Spree: (a) epiphyton dry weight per m2 artificial substrate, (b) light absorption by total (lines + circles) and 2-week epiphyton (lines), and (c) dry weight of submersed macrophytes per m2 river bottom (means standard deviation).
R2 ¼ 0:79;
(4)
or, using a hyperbolic curve fit: A¼
108 DW 9:2 þ DW
R2 ¼ 0:81:
(5)
A similar correlation (A = 110 DW/(12.7 + DW)) was found for the eutrophic shallow Lake Veluwe (The Netherlands) by Van Dijk (1993). Table 2 Differences in accumulating (‘‘total’’) epiphyton (dry weight, chlorophyll a (chl a) and percentage of light absorption) grown on artificial substrates as well as in macrophyte biomass at a sunny and a shaded site in the River Spree, analysed using a repeated measures ANOVA with site as between and time as within-subjects factors. Presented are means and standard deviation over the observation period (26 May to 11 October). Parameter
Site
Mean SD
n
ANOVA
df
Dry weight (g m2)
Sun Shade
14.3 12.3 12.7 6.7
10
Date Date site Site
9 9 1
4.09 5.82 1.04
<0.001 <0.001 0.348
Chl a (g m2)
Sun Shade
18.8 9.5 22.2 8.2
10
Date Date site Site
9 9 1
9.68 9.55 5.91
<0.001 <0.001 0.051
Chlorophytes chl a (mg m2)
Sun Shade
5.5 4.7 1.8 0.9
10
Date Date site Site
9 9 1
6.46 5.16 64.2
<0.001 <0.001 <0.001
Diatoms chl a (mg m2)
Sun Shade
13.4 7.2 20.5 7.8
10
Date Date site Site
9 9 1
15.4 6.28 19.1
<0.001 <0.001 0.005
Light absorption by epiphyton (%)
Sun Shade
61.5 17.1 71.2 15.0
10
Date Date site Site
9 9 1
63.8 7.19 27.9
<0.001 <0.001 0.002
Dry weight of submersed macrophytes (g m2)
Sun Shade
176 103 43.5 33.9
6
Date Date site Site
5 5 1
F
p
157 69.4 408
<0.001 <0.001 <0.001
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J. Ko¨hler et al. / Aquatic Botany 92 (2010) 129–136
sunny sites (14.9–17.2 E m2 d1), the average macrophyte biomass differed significantly between these groups (1967 423 g m2 versus 2805 826 g m2, one-way ANOVA: F = 10.6, p = 0.003). 4. Discussion 4.1. Light requirements of macrophyte growth
Fig. 4. Relation between light supply (average from May to July 2006) and biomass of macrophytes at transects with different canopy cover at the lower Spree. The line indicates the modelled relation (Eq. (6)).
Assuming a water layer of 0.5 m above the plants, shading by 2-week epiphyton and no self-shading by neighbouring aquatic vegetation, submersed macrophytes at the sunny river site on average received significantly more light (14.5 6.6 E m2 d1) than those at the shaded river site (2.4 0.7 E m2 d1, Fig. 1, Table 1). At the sunny river site, light supply to submersed macrophytes was lowest in May due to the spring peak in phytoplankton biomass. It increased in summer because of lower phytoplankton biomass and higher global radiation. At the shaded site, light supply to macrophytes was rather constant during the exposure period due to the inverse seasonal courses of shading by bank vegetation and light attenuation by phytoplankton. 3.5. Development of submersed macrophytes Submersed macrophytes (S. sagittifolia accompanied by Nuphar lutea (L.) SM., R. fluitans, P. pectinatus, C. demersum, M. spicatum and Sparganium emersum Rehmann) mainly sprouted from overwintering rhizomes (except for P. pectinatus) in late April (sunny site) or May (shaded site). Maximum aboveground biomass of submersed macrophytes was reached in July (shade, 85 30 g DW m2) or August (sun, 306 29 g DW m2). Macrophyte dry weight differed significantly between the two sites (Table 2). At the end of the study period (mid-October), most of the aboveground biomass had disappeared at both sites (Fig. 2c). The spatial heterogeneity in biomass distribution of submersed aquatic vegetation, found during mapping of 28 transects in July 2006, was explained to a large extend (R2 = 0.68) by different tree canopy cover when using an exponential biomass-light model, assuming a light compensation intensity I0 of 2 E m2 d1 given by Sand-Jensen and Borum (1991) (Fig. 4): B ¼ Bmax ð1 ea=ðII0 Þ=Bmax Þ;
(6)
where B and Bmax are the present and the maximum aboveground biomass, a is the initial slope and I the light intensity available to macrophytes in 0.5 m depth covered with 2-week epiphyton. Bmax was computed as 3400 159 g FW m2 and a as 890 116 g FW d E1. The coefficient of light saturation (Ik = I0 + Bmax/a) was estimated as 5.8 0.6 E m2 d1. About 50% of the maximum biomass were obtained at 4.7 E m2 d1 (‘‘half-saturating light intensity’’). A linear regression gave a poorer fit (R2 = 0.23) with significantly higher variance (F = 3.7, p < 0.001). The dominant species S. sagittifolia attained a maximum biomass above 1000 g FW m2 at a mean light supply of 3.1 E m2 d1. When pooling the transects into shaded (3.0–7.5 E m2 d1) and mostly
The half-saturating light intensity of submersed macrophytes in the lower Spree was estimated at 4.7 E m2 d1 (assuming light absorption by a 0.5 m water column and 2-week epiphyton). This fits very well to the half-saturating light intensity of about 4.5 E m2 d1 as was found for Zostera noltii by Vermaat and Verhagen (1996). The minimum daily light supply for submersed macrophytes often ranges between 2–4 E m2 (Sand-Jensen and Borum, 1991). The mean light supply at the maximum depth of growth ranged between about 1.6 E m2 d1 for caulescent and about 5 E m2 d1 for rosette-type angiosperms at a wide range of lakes (Middelboe and Markager, 1997). We found a saturation-type relation between light supply and macrophyte biomass (Fig. 4) in contrast to Sand-Jensen et al. (1989) who suggested a linear relationship between the relative growth rate (or log biomass) of submersed macrophytes and the available photon flux density in a Danish lowland stream. They included a biomass-dependent self-shading of macrophytes in their calculation of light availability inside the stands so that biomass increase was slowed down at higher external light intensities. In this way, growth of macrophytes was probably also light-saturated at a certain external light intensity in the Danish stream. Significant reduction in macrophyte biomass (20%) was only detected at high shading levels above 55% (Eq. (6)). Planting and sustaining trees at the riverside as a management tool for the control of extensive macrophyte growth thus requires the maintenance of a rather high tree density. 4.2. Relative importance of shading by bank vegetation, seston and epiphyton The exponential light dependency of aboveground biomass of submersed macrophytes found in our study implies that the importance of seston and epiphyton shading is different at sunny and shaded sites. As long as the available light intensity is still saturating (>Ik), light absorption by seston or epiphyton does not matter. When light supply becomes limiting, however, any additional shading should result in a lower biomass of submersed macrophytes. At the sunny site of our river, macrophytes covered by total epiphyton received light intensities above Ik (5.8 E m2 d1) in a depth of 0.5 m until mid September. Light intensities at 0.5 m depth always exceeded the assumed light compensation intensity of 2 E m2 d1. Light absorption by suspended and by attached algae thus shortened the period of optimum light supply but never prevented positive growth rates of submersed macrophytes at the sunny river site. At the shaded site, light intensity at the water surface exceeded Ik (5.8 E m2 d1) until the end of July. Light intensity available to macrophyte leaves covered by 2-week epiphyton was always below Ik in 0.5 m depth. Light intensities below 2 E m2 d1 were available to macrophyte leaves covered by 2-week epiphyton in September–October and by total epiphyton from mid-June onwards. In other words, shading by seston and epiphyton often made the difference between light-saturated and light-limited growth or even between positive and negative growth rates. Additional light absorption of phytoplankton in the water column
J. Ko¨hler et al. / Aquatic Botany 92 (2010) 129–136
and by epiphytic biofilm was thus crucial for the macrophyte development at shaded sites. The relative importance of the three attenuation components followed a distinct seasonal course. In spring, most light was attenuated by phytoplankton in the water column, whereas shading by bank trees and epiphyton was still low. Lowering the water level and/or reducing the phytoplankton concentration in this period would support growth of macrophytes. During summer, shading effects of bank vegetation dominated, and epiphyton absorbed more light than phytoplankton due to the particle-retaining effect of submersed macrophytes. A similar shift between planktonic and epiphytic algae was found in the more turbid river Vecht by Vermaat and De Bruyne (1993). We measured biomass and light absorption of epiphytic biofilm using an artificial substrate. Similar studies on real plants would face methodological problems (complete separation of epiphytic algae and host plant, estimation of their surface area) and inherent uncertainties (unknown age of the epiphytic biofilm, heterogeneous growth conditions within macrophyte stands). The validity of our approach was confirmed by the comparison of diatom pigments of plant pieces and artificial substrate at the end of the season. They revealed insignificant differences in diatom biomass (pigments of chlorophytes and host plants cannot be separated) in most cases and thus the general applicability of our approach. In general, host specificity of epiphyton seems low in eutrophic waters (Eminson and Moss, 1980). 4.3. Feedback effect of macrophytes on turbidity The net retention of particles and phytoplankton was much higher along the river course during the vegetation period than in the rest of the year. This retention considerably reduced turbidity. Although the contributions of sedimentation and grazing on particle losses are not clear, these retentive processes are caused or at least facilitated by aquatic vegetation. In this way, macrophytes improve their own light supply. More light may potentially enable faster growth and a higher final biomass of submersed macrophytes, which may retain even more particles. Such positive feedback between the abundance of submersed macrophytes and water clarity was already postulated for shallow lakes by Scheffer et al. (1993). In the Spree, this process was found to be relevant for submersed macrophyte growth only at the shaded sites. At sunny sites, light supply would suffice even at high phytoplankton concentrations in 0.5 m depth in summer (when particle retention is significant). According to Eq. (6), the improved water transparency along the 30 km river course supported a 61% higher biomass of macrophytes at shaded sites, but only 1% increase at sunny sites. Due to this saturation-type relationship between biomass and light supply, particle retention supported a more than 10% higher macrophyte biomass only at transects with more than 60% shading by bank vegetation. Additionally, the Spree was dominated by macrophyte species with long leaves or stems. Large parts float near the water surface making plant development nearly independent of water turbidity except for the early stages. In short: the improvement of the light supply by particle retention in macrophyte stands considerably improved submersed plant development in shaded parts of the Spree during summer but was unimportant in sunny regions and during spring. This feedback effect gains importance with increasing water depth and initial particle concentration. 4.4. Compensatory effects of tree shading on epiphyton growth We found that light absorption by epiphyton at the shaded site was significantly higher than at the sunny site. Shading effects by
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the bank tree canopy were thus not compensated by lower light absorption of the epiphytic biofilm at the shaded site. There are several possible reasons for the lack of decline in epiphyton biomass with reduced light supply. Generally, unicellular algae require less light than rooted macrophytes (SandJensen and Borum, 1991). Tuji (2000) found half of the maximum growth rate of benthic diatoms at light intensities of 5– 64 mE m2 s1 (0.25–3.2 E m2 d1 at 14 h of light per day). Rier et al. (2006) measured maximum growth of acclimated phytobenthos (mainly diatoms) at PAR > 2.5 E m2 d1. In the Spree, the upper layer of the epiphyton exposed at the shaded site in 0.5 m depth received more than 2 E m2 d1 nearly every day until mid September. In addition, the chl a to C ratio as a rough indicator for light adaptation was slightly lower at the shaded than the sunny site (Table 1). Taking these arguments together, it is highly probable that epiphyton growth was light-saturated even at the shaded site. Alternatively, high grazing pressure could explain the lacking correlation between epiphyton biomass and light (Hill, 1996). Feminella et al. (1989), Steinman (1992) and Hill et al. (1995) found biomass responses to increased light in shaded streams only after the removal of grazers. Epiphyton biomass in the Spree was significantly lower than that of downstream flushed Lake Mu¨ggelsee (Roberts et al., 2003) where predation pressure of omnivorous fish on epiphyton-grazing invertebrates is high (Okun et al., 2005). For eutrophic shallow lakes, Jones and Sayer (2003) showed that fish predation has a cascading effect on epiphytongrazing invertebrates, influencing the biomass of epiphyton and submersed plants. Direct evidence for epiphyton control by invertebrate grazing pressure in the River Spree is still lacking, so this possibility remains speculative. Epiphyton biomass was most probably not controlled by nutrient supply. Nutrient concentrations were always sufficiently high for maximum epiphyton growth (SRP > 10 mg L1, DIN > 100 mg L1, DSi > 2 mg L1, DIC > 20 mg L1). Flow favours rather than limits epiphyton accumulation and productivity (Horner et al., 1990) in the investigated velocity range of the Spree (below 40 cm s1). Therefore, epiphyton biomass was probably not controlled by high abrasive losses. This study quantified the importance of interacting effects of bank vegetation, epiphyton and suspended particles on light supply of aquatic vegetation. One of the emerging challenges is to analyse the cascading effects from fish to macroinvertebrate scrapers to epiphyton and eventually submersed macrophyte development in eutrophic lowland rivers. Acknowledgements We thank Marianne Graupe, Hanna Winkler, Barbara Meinck, Reinhard Ho¨lzel, Bernd Schu¨tze, Thomas Hintze, Christiane Herzog, Antje Lu¨der, Elke Zwirnmann, Hans-Ju¨rgen Exner and Thomas Rossoll for technical support. Jan Vermaat, Dean DeNicola, Tom Shatwell and two anonymous reviewers improved the manuscript. The study was financially supported by a grant from the Deutsche Bundesstiftung Umwelt and the Nowicki Foundation to J. Hachoł. References Anonymous, 2005. Deutsche Einheitsverfahren zur Wasser- Abwasser- und Schlamm-Untersuchung. Verlag Chemie, Weilheim. Asaeda, T., Sultana, M., Manatunge, J., Fujino, T., 2004. The effect of epiphytic algae on the growth and production of Potamogeton perfoliatus L. in two light conditions. Environ. Exp. Bot. 52, 225–238. Baker, K.S., Frouin, R., 1987. Relation between photosynthetically radiation and total insolation at the ocean surface under clear skies. Limnol. Oceanogr. 32, 1370– 1377. Bricaud, A., Stramski, D., 1990. Spectral absorption coefficients of living phytoplankton and nonalgal biogenous matter: a comparison between the Peru upwelling area and the Sargasso Sea. Limnol. Oceanogr. 35, 562–582.
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Chambers, P.A., Kalff, J., 1985. Depth distribution and biomass of submersed aquatic macrophyte communities in relation to Secchi depth. Can. J. Fish. Aquat. Sci. 42, 701–709. Davies-Colley, R.J., Quinn, J.M., 1998. Stream lighting in five regions of North Island, New Zealand: control by channel size and riparian vegetation. N. Z. J. Mar. Freshwater Res. 32, 591–605. Dawson, F.H., Kern-Hansen, U., 1979. The effect of natural and artificial shade on the macrophytes of lowland streams and the use of shade as a management technique. Int. Rev. Hydrobiol. 64, 437–455. Eminson, D., Moss, B., 1980. The composition and ecology of periphyton communities in freshwaters. I. The influence of host type and external environment on community composition. Br. Phycol. J. 15, 429–446. Feminella, J.W., Power, M.E., Resh, V.H., 1989. Periphyton responses to invertebrate grazing and riparian canopy in three northern California coastal streams. Freshwater Biol. 22, 445–457. Fietz, S., Nicklisch, A., 2004. An HPLC analysis of the summer phytoplankton assemblage in Lake Baikal. Freshwater Biol. 49, 332–345. Hill, W.R., 1996. Effects of light. In: Stevenson, R.J., Bothwell, M.L., Lowe, R.L. (Eds.), Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, pp. 121–148. Hill, W.R., Ryon, M.G., Schilling, E.M., 1995. Light limitation in a stream ecosystem: responses by primary producers and consumers. Ecology 76, 1297–1309. Hill, W.R., Mulholland, P.J., Marzolf, E.R., 2001. Stream ecosystem responses to forest leaf emergence in spring. Ecology 82, 2306–2319. Horner, R.R., Welch, E.B., Seeley, M.R., Jacoby, J.M., 1990. Responses of periphyton to changes in current velocity, suspended sediment and phosphorus concentration. Freshwater Biol. 24, 215–232. Hudon, C., Lalonde, S., Gagnon, P., 2000. Ranking the effects of site exposure, plant growth form, water depth, and transparency on aquatic plant biomass. Can. J. Fish. Aquat. Sci. 57, 31–42. Jones, J.I., Sayer, C., 2003. Does fish-invertebrate-periphyton cascade precipitate plant loss in shallow lakes? Ecology 84, 2155–2167. Ko¨hler, J., Hoeg, S., 2000. Phytoplankton selection in a river-lake system during two decades of changing nutrient supply. Hydrobiologia 424, 13–24. Middelboe, A.L., Markager, S., 1997. Depth limits and minimum light requirements of freshwater macrophytes. Freshwater Biol. 37, 553–568. Okun, N., Lewin, W.-C., Mehner, T., 2005. Top-down and bottom-up impacts of juvenile fish in a littoral reed stand. Freshwater Biol. 50, 798–812. Quinn, J.M., Phillips, N.R., Parkyn, S.M., 2007. Factors influencing retention of coarse particulate organic matter in streams. Earth Surf. Process. Landforms 32, 1186– 1203. Rier, S.T., Stevenson, R.J., LaLiberte, G.D., 2006. Photo-acclimation response of benthic stream algae across experimentally manipulated light gradients: a
comparison of growth rates and net primary productivity. J. Phycol. 42, 560– 567. Roberts, E., Kroker, J., Ko¨rner, S., Nicklisch, A., 2003. The role of periphyton during the re-colonization of a shallow lake with submerged macrophytes. Hydrobiologia 506, 525–530. Sand-Jensen, K., Borum, J., 1991. Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquat. Bot. 41, 137–175. Sand-Jensen, K., Søndergaard, M., 1981. Phytoplankton and epiphyte development and their shading effect on submerged macrophytes in lakes of different nutrient status. Int. Rev. Hydrobiol. 66, 529–552. Sand-Jensen, K., Jeppesen, E., Nielsen, K., Van der Bijl, L., Hjermind, L., Nielsen, L.W., Iversen, T.M., 1989. Growth of macrophytes and ecosystem consequences in a Danish lowland stream. Freshwater Biol. 22, 15–32. Sand-Jensen, K., Riis, T., Vestergaard, O., Larsen, S.E., 2000. Macrophyte decline in Danish lakes and streams over the last 100 years. J. Ecol. 88, 1030–1040. Scheffer, M., Hosper, S.H., Meijer, M.L., Moss, B., Jeppesen, E., 1993. Alternative equilibria in shallow lakes. Trends Ecol. Evol. 8, 275–279. Schulz, M., Kozerski, H.P., Pluntke, T., Rinke, K., 2003. The influence of macrophytes on sedimentation and nutrient retention in the lower River Spree (Germany). Water Res. 37, 569–578. Schulz, M., Rinke, K., Ko¨hler, J., 2003. A combined approach of photogrammetrical methods and field studies to determine nutrient retention by submersed macrophytes in running waters. Aquat. Bot. 76, 17–29. Steinman, A.D., 1992. Does an increase in irradiance influence periphyton in a heavily grazed woodland stream? Oecologia 91, 163–170. Tuji, A., 2000. The effect of irradiance on the growth of different forms of freshwater diatoms: implications for succession in attached diatom communities. J. Phycol. 36, 659–661. Vannote, R.L., Minshall, G.W., Cummins, K.W., Sedell, J.R., Cushing, C.E., 1980. The river continuum concept. Can. J. Fish. Aquat. Sci. 37, 130–137. Van Dijk, G., 1993. Dynamics and attenuation characteristics of periphyton upon artificial substratum under various light conditions and some additional observations on periphyton upon Potamogeton pectinatus L. Hydrobiologia 252, 143– 161. Vermaat, J.E., De Bruyne, R.J., 1993. Factors limiting the distribution of submerged water plants in the lowland River Vecht (The Netherlands). Freshwater Biol. 30, 147–157. Vermaat, J.E., Verhagen, F.C.H., 1996. Seasonal variation in the intertidal seagrass Zostera noltii Hornem.: coupling demographic and physiological patterns. Aquat. Bot. 52, 259–281. Wright, J.F., Cameron, A.C., Hiley, P.D., Berrie, A.D., 1982. Seasonal-changes in biomass of macrophytes on shaded and unshaded sections of the River Lambourn, England. Freshwater Biol. 12, 271–283.
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Aquatic Botany journal homepage: www.elsevier.com/locate/aquabot
Regulation of submersed macrophyte biomass in a temperate lowland river: Interactions between shading by bank vegetation, epiphyton and water turbidity Jan Ko¨hler *, Justyna Hachoł 1, Sabine Hilt Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mu¨ggelseedamm 301, 12587 Berlin, Germany
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 June 2009 Received in revised form 21 October 2009 Accepted 30 October 2009 Available online 5 November 2009
Growth of aquatic vegetation is often controlled by light supply, which is potentially decreased by bank vegetation, water turbidity and epiphytic biofilm. To understand the relative importance of these shading factors and the interactions between them we analysed the seasonal course of macrophyte biomass, shading by bank vegetation, turbidity of the water column and epiphytic light absorption in shaded and sunny sections of a temperate eutrophic lowland river. At a shaded site, bank vegetation decreased the light supply by 79%, 0.5 m water column by 45% and 2-week-old epiphyton by 28% during the vegetation period. Growth of submersed macrophytes, but not of epiphyton, was light-limited in the shaded sections. We found a saturation-type correlation between light supply and macrophyte biomass. Therefore, the additional light absorption of the water column or epiphyton only shortened the period of optimum light supply at the sunny site, but was crucial for macrophyte development at the shaded site. Light absorption of phytoplankton was most important in spring and that of epiphyton in late summer. Submersed macrophytes effectively retained particles and thus improved light supply of downstream stands, but this positive feedback effect was only relevant for shaded sections in summer. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Aquatic vegetation Growth Light absorption Light limitation Microphytobenthos Phytoplankton retention
1. Introduction Macrophytes are a key component of aquatic communities in many streams and lowland rivers. Long-term (Sand-Jensen et al., 2000) as well as spatial changes (Vannote et al., 1980) in biomass and composition of aquatic vegetation are often caused by changes in light supply. In general, three different external factors control light supply of submersed macrophytes in rivers: shading by bank vegetation (Dawson and Kern-Hansen, 1979; Wright et al., 1982; Davies-Colley and Quinn, 1998), light absorption in the water column by suspended algae, mineral particles and dissolved coloured substances (Hudon et al., 2000) and light absorption of the epiphytic biofilm (Chambers and Kalff, 1985; Asaeda et al., 2004). These factors have usually been analysed separately; few studies have dealt with combined effects of water turbidity and epiphyton (e.g., Sand-Jensen and Søndergaard, 1981; Vermaat and De Bruyne, 1993). However, the single attenuation components are not independent and interact in different ways. Shading by bank vegetation may not only limit growth of submersed macrophytes but also that
* Corresponding author. Tel.: +49 30 64181687; fax: +49 30 64181682. E-mail addresses: [email protected] (J. Ko¨hler), [email protected] (J. Hachoł), [email protected] (S. Hilt). 1 Present address: Institute of Environmental Development and Protection, University of Environmental and Life Sciences, Pl. Grunwaldzki 24, 50-363 Wroclaw, Poland. 0304-3770/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2009.10.018
of epiphyton (e.g., Hill et al., 2001), potentially resulting in an inverse relation between shading by trees and light absorption by epiphyton. Phytoplankton shades both epiphyton and submersed macrophytes, which potentially counterbalances the overall effect of phytoplankton shading. In addition, concentrations of phytoplankton and other suspended particles often decline during passage of macrophyte stands (e.g., Schulz et al., 2003a; Quinn et al., 2007). Therefore, density of macrophyte stands and light attenuation of the water column are potentially inversely related. This positive feedback could support growth of submersed macrophytes at downstream sites but might be compensated by higher epiphyton biomass if epiphyton growth is light-limited. All these effects are subject to distinct seasonal changes. Additionally, the importance of shading effects on macrophyte growth depends on the relation between growth and light supply. A linear relation, as was found by Dawson and Kern-Hansen (1979) and Sand-Jensen et al. (1989), would imply a similar relative decline in growth rate by any additional shading. In the case of a saturation-type relation between light and growth (e.g., Vermaat and Verhagen, 1996), however, additional shading would have no effect at saturating light intensities, but could be crucial at light limitation. Here, we compared annual courses of light supply and development of submersed macrophytes, epiphyton and phytoplankton at a sunny and a shaded site as well as maximum macrophyte biomass at 28 transects of different shading grade in a eutrophic, medium-sized, temperate lowland river to test the following hypotheses:
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(1) The relation between biomass of submersed macrophytes and light supply is non-linear, i.e. effects of additional shading depend on present light intensity. (2) Growth of submersed macrophytes in medium-sized lowland rivers is mainly influenced by shading from bank vegetation; shading by phytoplankton and epiphyton may additionally limit growth at certain times and water depths. (3) The shading effect of bank vegetation on submersed macrophytes is partly compensated by lower biomass and thus less shading of (light-limited) epiphyton. (4) Submersed macrophytes improve their own light supply by retaining suspended particles, but this positive feedback is also partly compensated by higher epiphyton biomass. 2. Methods 2.1. Study site The Spree is a eutrophic lowland river in North-Eastern Germany. It originates in the Lusatian Mountains (Saxony) and flows for 380 km through several reservoirs and shallow lakes to Berlin. There, the River Spree merges with the Havel, a tributary of the Elbe river (detailed description in Ko¨hler and Hoeg, 2000). The lower part of the Spree system, where this study was carried out, follows a former glacial spillway. The channel has a mean slope of about 0.13% and a width between 20 and 50 m. At mean discharge, 73% of the river course (river-km 302–334) is deeper than 1.0 m, 39% deeper than 1.5 m, and 9% deeper than 2.0 m. The river water level is measured daily by the Waterways and Shipping Administration Berlin (km 302) and by the State Department of Environment Brandenburg (km 328). These authorities estimated daily discharge from regularly updated stage–discharge relationships. Depths and volume of the water body were calculated from about 300 cross-section profiles of water depth and the daily water levels. The mean flow velocity was estimated from the volume of the water body, rate of discharge and length of the river stretch between the gauges. We conducted measurements at one shaded and two sunny transects of the River Spree. At the shaded site both banks were densely lined with trees (mainly black alder (Alnus glutinosa (L.) Gaertn.) and poplar (Populus canescens (Aiton) SM.), whereas only some trees were present on the northern bank of the sunny sites. 2.2. Macrophyte biomass Cover of the main species of submersed macrophytes was mapped monthly between May and October 2006 at a sunny (river-km 321) and a shaded (river-km 322) transect. Additionally, 28 transects covering a range of shading grades were mapped in July 2006. At each transect, a boat was moved between two ropes across the river to map a 6 m swath over the whole breadth of the river. Cover of each species was estimated visually in a grid of 1 m 2 m at three depths (bottom, middle and surface) using four classes: 0–10%, 10–40%, 40–70% and 70– 100%. The aboveground biomass of submersed macrophyte stands was harvested in July 2006 by diving using a 0.5 m 0.5 m metal frame. Macrophytes were separated into species, weighed and dried at 70 8C until weight constancy to determine dry weight (DW). Fresh weight (FW) of the harvested stands was correlated with the estimated cover and this speciesspecific ratio (biomass per relative cover) was used to calculate the fresh weight of each abundant species per m2 river bottom. In order to have at least ten replicates per species, the results of analogous harvests in 2001 (Schulz et al., 2003b) and in 2005 (J. Ko¨hler, Unpublished data) were included in the calculation of biomass per cover ratios.
2.3. Epiphyton biomass Epiphyton biomass was measured on artificial substrate exposed at a shaded site (km 322) and at a sunny site (km 315). Exposure was started on 26 April 2006, and epiphyton samples were collected fortnightly from 10 May to 11 October 2006. Epiphyton grows on both old and fresh leaves of submersed plants so we measured its biomass after 2 weeks exposure in consecutively repeating intervals (hereafter called ‘‘2-week epiphyton’’) as well as after 4–24 weeks exposure) from 26 April till the date of subsampling (hereafter called ‘‘total epiphyton’’). A similar approach was described in Vermaat and De Bruyne (1993). Artificial substrate consisted of transparent polypropylene sheets with a slightly textured surface (IBICO1, Germany). A4 (210 mm 297 mm) sheets were subdivided into ten strips held together like a comb. Substrates were placed in macrophyte-free areas and suspended 50 cm below the water surface. The sheets were fixed at the upstream side between small aluminium fillets and kept in horizontal position by the current. Every second week, four strips of the total epiphyton and the 2-week epiphyton series were sampled per site. Additionally, five pieces of Sagittaria sagittifolia L. (1.13 cm2 each) were collected at both river sites for pigment analyses at 15 August and 6 September 2006. Each substrate strip was slid into a separate damp plastic container, which was placed in a dark thermobox with some water at its bottom to provide 100% humidity during transport to the lab. Within hours of sample collection, the epiphyton was scrubbed from the substrate using a toothbrush, and suspended in a defined amount of GF/F-filtered river water. After homogenization, subsamples of each suspension were filtered onto three GF/F glass-fibre filters. One pre-weighed and pre-washed filter was dried at 105 8C to analyse dry weight and the contents of organic carbon and nitrogen as described below. One filter was frozen at 80 8C for later HPLC analysis and a third one used for absorption measurements. For pigment analyses, filters and plant pieces were freeze-dried and pigments were extracted by vibration shaking (2000 rpm, 1.5 h) with dimethylformamide and glass beads (0.75–1.0 mm diameter). After centrifugation for 20 min (2500 g, 4 8C), pigments were separated, identified and quantified with a HPLC system (Waters, USA) as described by Fietz and Nicklisch (2004). Fucoxanthin and chlorophyll b were used as marker pigments for diatoms and chlorophytes, respectively. Algae from other groups with the same marker pigments were not detected by microscopic analysis. We estimated the relative contributions of diatoms and chlorophytes to total epiphyton chl a by multiple linear regression (see, e.g., Fietz and Nicklisch, 2004): chl a ¼ 2:456 fucoxanthin þ 3:437 chlorophyll b R2 ¼ 0:99; p < 0:001:
(1)
The high coefficient of determination proofs a nearly constant ratio of marker pigment to chl a within the algal group. Epiphyton biomass was always related to the area of the artificial substrate. Immediately after filtration, the wet ‘‘absorption filter’’ was used to measure light absorption spectra (against blank wet filter) in a double-beam spectrophotometer (Shimadzu UV-VIS 2101). The mean optical density at 740–760 nm (OD740–760) was subtracted, filter effects were corrected according to Bricaud and Stramski (1990) and the absorption coefficient of the particles (a) was calculated as a ¼ ðODl OD740760 Þ
AF V S AS V F
(2)
where ODl is the optical density at a given wavelength, AF the clearance area of the filter, AS the area of the substrate strip, and VS
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and VF are the volumes of the epiphyton suspension per strip and of the filtered suspension, respectively. The percent light absorption (A) of epiphyton was calculated as A ¼ 100 ð1 10a Þ
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homogeneity of variance and log-transformed where necessary. Transformation satisfied the requirements in all cases. All analyses were carried out using the statistical package SPSS 14.0 (SPSS Inc., Chicago, IL).
(3) 3. Results
and averaged for 400–700 nm. 2.4. Light availability Global radiation was continuously recorded from a monitoring station at Lake Mu¨ggelsee, about 20 km downstream of the river sites. Photosynthetically available radiation (PAR) was calculated as 46% of net global radiation (=gross global radiation minus reflection and backscattering, see Baker and Frouin, 1987). The shading effect of riverbank vegetation was continuously recorded with a cosine-corrected PAR sensor (Li-Cor Biosciences, Lincoln, Nebraska) at the shaded exposure site. Underwater light extinction was calculated from light intensities simultaneously measured with spherical quantum sensors (Li-Cor Biosciences) in two water depths using the Lambert–Beer law. Light intensity at the 28 transects, where macrophytes were mapped in July, was calculated from measured intensities at the sunny and the shaded site and the canopy cover of bank trees estimated from aerial photographs. PAR attenuation by seston and epiphyton was interpolated between sampling dates. Interpolated attenuation data and continuously measured global radiation were used to calculate daily means of light availability at the water surface, for epiphyton growth in 0.5 m depth (net PAR multiplied by the percent light attenuated by the water layer) and for macrophytes (as above, then multiplied by percent light absorption of epiphyton). 2.5. Seston, nutrient availability, pH and water temperature Water samples were collected fortnightly at the beginning (river-km 302) and the end (km 332) of the river course, which did not receive any tributaries or wastewater inflows. The average value of both sites was used for our analyses. Water temperature and pH were measured immediately after sampling (pH probe, WTW, Weilheim, Germany). In the laboratory, two subsamples were filtered onto pre-washed and pre-weighed GF/F glass-fibre filters as described above, dried at 105 8C overnight and weighed to determine seston DW. Nitrogen (N) and carbon (C) content were determined using a Vario EL analyser (Elementar) after removing the carbonates by treatment with HCl. Each filter was wetted with some drops of 0.5 M HCl until no more foaming occurred and was allowed to dry overnight at 36 8C. Nutrient concentrations (total phosphorus: TP, soluble reactive phosphorus: SRP, total nitrogen: TN, dissolved inorganic nitrogen: DIN (=nitrate + ammonium), dissolved reactive silica: DSi, dissolved inorganic carbon: DIC), were measured using standard methods (Anonymous, 2005). Phytoplankton pigments were analysed in subsamples concentrated on GF/F filters as described for epiphyton pigments. 2.6. Statistical analyses Differences between the two river sites were tested by analyses of variance (ANOVA). We used a repeated measure ANOVA with time as the within-subjects factor and site as the between-subjects factor. Maximum biomass data of submersed macrophytes at 28 sites were compared using a one-way ANOVA and subsequent multiple comparisons with Tukey’s post hoc test at p < 0.05. Significance of changes in nutrient concentrations, discharge and water temperature between the exposure sites was tested by paired-samples t-tests at p < 0.05, assuming a linear change along the whole river course. All data were tested for normality and
3.1. Nutrient availability, pH, water temperature and hydrological conditions Concentrations of SRP during the investigated period averaged at 58 21 (standard deviation) mg L1 and fell below 50 mg L1 only in spring (April–early May). The mean concentration of DIN was 337 105 mg L1, values below 100 mg L1 were not found. The molar N:P ratio (DIN:SRP) fell below 16 (‘‘Redfield ratio’’) from June through early October, indicating a relative shortage in nitrogen. The concentrations of DSi and DIC were always higher than 2 and 20 mg L1, respectively. The pH averaged at 7.64 0.24. In epiphyton, the molar C:N ratios ranged between 5 and 7 in May and at the beginning of June and, in total epiphyton also in September–October (sun) and in October (shade). C:N ratios above 10 were only found in 2-week epiphyton (at August 15, sun, and in July, shade). In all other samples, C:N ratios ranged between 7 and 10. Monthly mean water temperature rose from 10.6 8C in April to 23.4 8C in July and declined to 14.0 8C in mid-October. The water discharge declined from April (15.6 1.7 m3 s1) to July–August 2006 (2.6 0.9 m3 s1). It increased again in September–October to 5.8 1.5 m3 s1. Due to the impounding effects of downstream lakes and dense stands of aquatic vegetation in the river, the mean depth of the river stretch was only slightly higher in April (1.42 0.04 m) than in July–August (1.22 0.08 m) and in September–October (1.30 0.06 m). Therefore, the mean velocity of flow paralleled the seasonal course of discharge. Monthly averages of flow velocity declined from 36 1 cm s1 in April to 8 2 cm s1 in July and August and increased again to 21 3 cm s1 in October 2006. On average, concentrations of TP and DSi as well as water temperature and discharge did not significantly change between sites. The mean concentrations of SRP (+11%) and of DIN (+7%) increased whereas TN declined (2%) from the sunny to the shaded site. 3.2. Light availability for epiphyton Net PAR (gross PAR minus albedo) averaged at 33.8 E m2 d1 (sunny site) and at 6.4 E m2 d1 (shade) at the water surface during the exposure period. Global radiation was reduced by cloudy periods mainly in the second half of May and in August but was 20–38% higher than the long-term average (1976–2005) in the first half of May, in June–July and September 2006. Bank vegetation reduced the mean light intensity at the shaded site by about 60%, at the beginning and the end of the exposure period, and by 83 4%, in July–August (Fig. 1). At the beginning of the river course, phytoplankton attained a maximum chl a in early May (88 mg L1) and a mean chl a of only 18 mg L1 in June–July. Seston DW was also highest in late spring (14.8 mg L1 at May 9) and lowest in June–July (5.3 0.4 mg L1). It increased again in late summer to autumn. Along the 30 km river section between km 302 and 332, phytoplankton chl a remained nearly constant in March–May but declined by 76 18% during passage in June–September. Accordingly, mean light attenuation in the water column declined from 1.45 0.17 to 1.04 0.12 m1 and mean light intensity in 0.5 m depth increased from 17.0 7.5 to 20.9 8.6 E m2 d1 along this river stretch (no shade by bank vegetation, average of June–September). On average of the whole river section, the mean coefficient of vertical light attenuation declined from 3.07 m1 (first half of May) to 1.07 m1 in June and
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Fig. 1. Light intensity (PAR) at the water surface (solid line), in 0.5 m depth (dotted line) and available for submersed macrophytes in 0.5 m depth covered by 2-week epiphyton (filled area) at the sunny (top) and the shaded site (bottom) of the Spree.
0.78 m1 in July–August and increased again to 1.27 m1 in September and 1.87 m1 in early October. During the exposure period, a 0.5 m water column attenuated on average 45 15% of the surface light intensity. The resulting PAR at a water depth of 0.5 m averaged at 18.7 E m2 d1 (sun) and 3.3 E m2 d1 (shade, Fig. 1, Table 1). 3.3. Development of epiphyton Total epiphyton grew continuously at the sunny site of the river from May until August, reaching a maximum of 33.4 g DW
per m2 artificial substrate. At the shaded site, total epiphyton grew rapidly in May and June to 17.2 g DW m2, declined in July and grew again for the remaining exposure time (Fig. 2a). Total epiphyton DW and total chl a were not significantly different between both sites. Diatom chl a was higher and chlorophyte chl a was lower at the shaded than at the sunny site (Table 2). Dry weight, total chl a and diatom chl a of 2-week epiphyton were significantly higher at the shaded than at the sunny site (Fig. 2a, Table 1). Chlorophyte chl a and the ratio of particulate organic C to N did not differ. The relative proportion of chl a to C content was slightly lower at the shaded site, compared to the sunny one (Table 1). Net growth rates of epiphyton were calculated as chl a increase per day after 2 weeks of exposure. Diatoms attained highest net growth rates at the sunny river site in the first half of June (2.2 mg chl a m2 d1) and at the shaded site at the end of June (1.2 mg chl a m2 d1). Maximum growth of chlorophytes was found 2 weeks later, but their accrual rates never exceeded 0.5 mg chl a m2 d1. Biomass of epiphytic diatoms was estimated from fucoxanthin concentrations of S. sagittifolia pieces at two sampling dates. Diatom chl a per m2 leaf area averaged at 36.9 14.6 mg (sun), 25.2 5.0 mg (shade, 15 August) and 8.0 1.4 mg (6 September 2006, sun). Diatom chl a did not significantly differ between plastic strip and leaf at the shaded site at 15 August (p = 0.38) and at the sunny site at 6 September (p = 0.18). A significantly (p = 0.045) lower diatom chl a was found on the artificial substrate compared to the leaf at the sunny site at 15 August (15.4 4.2 mg m2).
Table 1 Mean dry weight, chlorophyll a (chl a, both per m2 of artificial substrate) and chemical composition of 2-week epiphyton grown on artificial substrates at a sunny and a shaded site in the River Spree between 26 May and 11 October and of light availability (PAR: photosynthetically active radiation—at the water surface, for epiphyton and for macrophyte growth in 0.5 m depth) between 29 April and 11 October, analysed using a repeated measures ANOVA with site as between and time as within subjects. Parameter
Site 2
n
ANOVA
df
F
p
Sun Shade
3.5 3.5 5.1 3.4
10
Date Date site Site
9 9 1
12.8 10.1 41.3
<0.001 <0.001 0.001
Chl a total (mg m2)
Sun Shade
8.0 8.2 12.3 9.4
10
Date Date site Site
9 9 1
30.4 26.6 18.1
<0.001 <0.001 0.005
Diatom chl a (mg m2)
Sun Shade
6.2 6.5 10.6 8.4
10
Date Date site Site
9 9 1
24.7 25.2 22.7
<0.001 <0.001 0.003
Chlorophytes chl a (mg m2)
Sun Shade
1.8 2.1 1.8 1.7
10
Date Date site Site
9 9 1
51.9 19.9 0.01
<0.001 <0.001 0.97
C/N (molar)
Sun Shade
8.2 1.6 8.6 1.5
10
Date Date site Site
9 9 1
61.6 28.1 5.3
<0.001 <0.001 0.06
Chl a/C
Sun Shade
93 72 70 54
10
Date Date site Site
9 9 1
26.2 37.7 11.0
<0.001 <0.001 0.016
Light absorption by periphyton (%)
Sun Shade
22.3 14.2 33.0 14.1
10
Date Date site Site
9 9 1
39.1 12.1 115
<0.001 <0.001 <0.001
PAR at water surface (E m2 d1)
Sun Shade
33.8 14.2 6.4 2.6
11
Date Date site Site
10 10 1
20.4 11.9 931
<0.001 <0.001 <0.001
PAR for periphyton (E m2 d1)
Sun Shade
18.7 10.1 3.3 1.2
11
Date Date site Site
10 10 1
34.5 22.8 903
<0.001 <0.001 <0.001
PAR for macrophytes (E m2 d1)
Sun Shade
14.5 6.6 2.4 0.8
11
Date Date site Site
10 10 1
17.3 13.4 1035
<0.001 <0.001 <0.001
Dry weight (g m
)
Mean SD
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133
Fig. 3. Percent PAR absorption plotted against dry weight of epiphyton on artificial substrate exposed in 0.5 m water depth and fitted exponential curve (Eq. (4)).
3.4. Light available to submersed macrophytes Light absorption by total epiphyton increased during the first 2 months (Fig. 2b). Between 26 April and 11 October, total epiphyton reduced the incoming PAR by 61 17% at the sunny and by 71 15% at the shaded river site (Table 2). Two-week epiphyton absorbed 22 14% (sun) and 33 14% (shade) of the incoming PAR, respectively. Mean light absorption of both total and 2-week epiphyton was significantly higher at the shaded than at the sunny site (Tables 1 and 2). The percentage of absorbed light (A) and epiphyton DW were highly significantly correlated (p < 0.001; Fig. 3): A ¼ 100 ð1 e0:083DW Þ Fig. 2. Development of epiphyton and submersed macrophytes at a sunny (solid lines) and a shaded site (dotted lines) in the River Spree: (a) epiphyton dry weight per m2 artificial substrate, (b) light absorption by total (lines + circles) and 2-week epiphyton (lines), and (c) dry weight of submersed macrophytes per m2 river bottom (means standard deviation).
R2 ¼ 0:79;
(4)
or, using a hyperbolic curve fit: A¼
108 DW 9:2 þ DW
R2 ¼ 0:81:
(5)
A similar correlation (A = 110 DW/(12.7 + DW)) was found for the eutrophic shallow Lake Veluwe (The Netherlands) by Van Dijk (1993). Table 2 Differences in accumulating (‘‘total’’) epiphyton (dry weight, chlorophyll a (chl a) and percentage of light absorption) grown on artificial substrates as well as in macrophyte biomass at a sunny and a shaded site in the River Spree, analysed using a repeated measures ANOVA with site as between and time as within-subjects factors. Presented are means and standard deviation over the observation period (26 May to 11 October). Parameter
Site
Mean SD
n
ANOVA
df
Dry weight (g m2)
Sun Shade
14.3 12.3 12.7 6.7
10
Date Date site Site
9 9 1
4.09 5.82 1.04
<0.001 <0.001 0.348
Chl a (g m2)
Sun Shade
18.8 9.5 22.2 8.2
10
Date Date site Site
9 9 1
9.68 9.55 5.91
<0.001 <0.001 0.051
Chlorophytes chl a (mg m2)
Sun Shade
5.5 4.7 1.8 0.9
10
Date Date site Site
9 9 1
6.46 5.16 64.2
<0.001 <0.001 <0.001
Diatoms chl a (mg m2)
Sun Shade
13.4 7.2 20.5 7.8
10
Date Date site Site
9 9 1
15.4 6.28 19.1
<0.001 <0.001 0.005
Light absorption by epiphyton (%)
Sun Shade
61.5 17.1 71.2 15.0
10
Date Date site Site
9 9 1
63.8 7.19 27.9
<0.001 <0.001 0.002
Dry weight of submersed macrophytes (g m2)
Sun Shade
176 103 43.5 33.9
6
Date Date site Site
5 5 1
F
p
157 69.4 408
<0.001 <0.001 <0.001
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J. Ko¨hler et al. / Aquatic Botany 92 (2010) 129–136
sunny sites (14.9–17.2 E m2 d1), the average macrophyte biomass differed significantly between these groups (1967 423 g m2 versus 2805 826 g m2, one-way ANOVA: F = 10.6, p = 0.003). 4. Discussion 4.1. Light requirements of macrophyte growth
Fig. 4. Relation between light supply (average from May to July 2006) and biomass of macrophytes at transects with different canopy cover at the lower Spree. The line indicates the modelled relation (Eq. (6)).
Assuming a water layer of 0.5 m above the plants, shading by 2-week epiphyton and no self-shading by neighbouring aquatic vegetation, submersed macrophytes at the sunny river site on average received significantly more light (14.5 6.6 E m2 d1) than those at the shaded river site (2.4 0.7 E m2 d1, Fig. 1, Table 1). At the sunny river site, light supply to submersed macrophytes was lowest in May due to the spring peak in phytoplankton biomass. It increased in summer because of lower phytoplankton biomass and higher global radiation. At the shaded site, light supply to macrophytes was rather constant during the exposure period due to the inverse seasonal courses of shading by bank vegetation and light attenuation by phytoplankton. 3.5. Development of submersed macrophytes Submersed macrophytes (S. sagittifolia accompanied by Nuphar lutea (L.) SM., R. fluitans, P. pectinatus, C. demersum, M. spicatum and Sparganium emersum Rehmann) mainly sprouted from overwintering rhizomes (except for P. pectinatus) in late April (sunny site) or May (shaded site). Maximum aboveground biomass of submersed macrophytes was reached in July (shade, 85 30 g DW m2) or August (sun, 306 29 g DW m2). Macrophyte dry weight differed significantly between the two sites (Table 2). At the end of the study period (mid-October), most of the aboveground biomass had disappeared at both sites (Fig. 2c). The spatial heterogeneity in biomass distribution of submersed aquatic vegetation, found during mapping of 28 transects in July 2006, was explained to a large extend (R2 = 0.68) by different tree canopy cover when using an exponential biomass-light model, assuming a light compensation intensity I0 of 2 E m2 d1 given by Sand-Jensen and Borum (1991) (Fig. 4): B ¼ Bmax ð1 ea=ðII0 Þ=Bmax Þ;
(6)
where B and Bmax are the present and the maximum aboveground biomass, a is the initial slope and I the light intensity available to macrophytes in 0.5 m depth covered with 2-week epiphyton. Bmax was computed as 3400 159 g FW m2 and a as 890 116 g FW d E1. The coefficient of light saturation (Ik = I0 + Bmax/a) was estimated as 5.8 0.6 E m2 d1. About 50% of the maximum biomass were obtained at 4.7 E m2 d1 (‘‘half-saturating light intensity’’). A linear regression gave a poorer fit (R2 = 0.23) with significantly higher variance (F = 3.7, p < 0.001). The dominant species S. sagittifolia attained a maximum biomass above 1000 g FW m2 at a mean light supply of 3.1 E m2 d1. When pooling the transects into shaded (3.0–7.5 E m2 d1) and mostly
The half-saturating light intensity of submersed macrophytes in the lower Spree was estimated at 4.7 E m2 d1 (assuming light absorption by a 0.5 m water column and 2-week epiphyton). This fits very well to the half-saturating light intensity of about 4.5 E m2 d1 as was found for Zostera noltii by Vermaat and Verhagen (1996). The minimum daily light supply for submersed macrophytes often ranges between 2–4 E m2 (Sand-Jensen and Borum, 1991). The mean light supply at the maximum depth of growth ranged between about 1.6 E m2 d1 for caulescent and about 5 E m2 d1 for rosette-type angiosperms at a wide range of lakes (Middelboe and Markager, 1997). We found a saturation-type relation between light supply and macrophyte biomass (Fig. 4) in contrast to Sand-Jensen et al. (1989) who suggested a linear relationship between the relative growth rate (or log biomass) of submersed macrophytes and the available photon flux density in a Danish lowland stream. They included a biomass-dependent self-shading of macrophytes in their calculation of light availability inside the stands so that biomass increase was slowed down at higher external light intensities. In this way, growth of macrophytes was probably also light-saturated at a certain external light intensity in the Danish stream. Significant reduction in macrophyte biomass (20%) was only detected at high shading levels above 55% (Eq. (6)). Planting and sustaining trees at the riverside as a management tool for the control of extensive macrophyte growth thus requires the maintenance of a rather high tree density. 4.2. Relative importance of shading by bank vegetation, seston and epiphyton The exponential light dependency of aboveground biomass of submersed macrophytes found in our study implies that the importance of seston and epiphyton shading is different at sunny and shaded sites. As long as the available light intensity is still saturating (>Ik), light absorption by seston or epiphyton does not matter. When light supply becomes limiting, however, any additional shading should result in a lower biomass of submersed macrophytes. At the sunny site of our river, macrophytes covered by total epiphyton received light intensities above Ik (5.8 E m2 d1) in a depth of 0.5 m until mid September. Light intensities at 0.5 m depth always exceeded the assumed light compensation intensity of 2 E m2 d1. Light absorption by suspended and by attached algae thus shortened the period of optimum light supply but never prevented positive growth rates of submersed macrophytes at the sunny river site. At the shaded site, light intensity at the water surface exceeded Ik (5.8 E m2 d1) until the end of July. Light intensity available to macrophyte leaves covered by 2-week epiphyton was always below Ik in 0.5 m depth. Light intensities below 2 E m2 d1 were available to macrophyte leaves covered by 2-week epiphyton in September–October and by total epiphyton from mid-June onwards. In other words, shading by seston and epiphyton often made the difference between light-saturated and light-limited growth or even between positive and negative growth rates. Additional light absorption of phytoplankton in the water column
J. Ko¨hler et al. / Aquatic Botany 92 (2010) 129–136
and by epiphytic biofilm was thus crucial for the macrophyte development at shaded sites. The relative importance of the three attenuation components followed a distinct seasonal course. In spring, most light was attenuated by phytoplankton in the water column, whereas shading by bank trees and epiphyton was still low. Lowering the water level and/or reducing the phytoplankton concentration in this period would support growth of macrophytes. During summer, shading effects of bank vegetation dominated, and epiphyton absorbed more light than phytoplankton due to the particle-retaining effect of submersed macrophytes. A similar shift between planktonic and epiphytic algae was found in the more turbid river Vecht by Vermaat and De Bruyne (1993). We measured biomass and light absorption of epiphytic biofilm using an artificial substrate. Similar studies on real plants would face methodological problems (complete separation of epiphytic algae and host plant, estimation of their surface area) and inherent uncertainties (unknown age of the epiphytic biofilm, heterogeneous growth conditions within macrophyte stands). The validity of our approach was confirmed by the comparison of diatom pigments of plant pieces and artificial substrate at the end of the season. They revealed insignificant differences in diatom biomass (pigments of chlorophytes and host plants cannot be separated) in most cases and thus the general applicability of our approach. In general, host specificity of epiphyton seems low in eutrophic waters (Eminson and Moss, 1980). 4.3. Feedback effect of macrophytes on turbidity The net retention of particles and phytoplankton was much higher along the river course during the vegetation period than in the rest of the year. This retention considerably reduced turbidity. Although the contributions of sedimentation and grazing on particle losses are not clear, these retentive processes are caused or at least facilitated by aquatic vegetation. In this way, macrophytes improve their own light supply. More light may potentially enable faster growth and a higher final biomass of submersed macrophytes, which may retain even more particles. Such positive feedback between the abundance of submersed macrophytes and water clarity was already postulated for shallow lakes by Scheffer et al. (1993). In the Spree, this process was found to be relevant for submersed macrophyte growth only at the shaded sites. At sunny sites, light supply would suffice even at high phytoplankton concentrations in 0.5 m depth in summer (when particle retention is significant). According to Eq. (6), the improved water transparency along the 30 km river course supported a 61% higher biomass of macrophytes at shaded sites, but only 1% increase at sunny sites. Due to this saturation-type relationship between biomass and light supply, particle retention supported a more than 10% higher macrophyte biomass only at transects with more than 60% shading by bank vegetation. Additionally, the Spree was dominated by macrophyte species with long leaves or stems. Large parts float near the water surface making plant development nearly independent of water turbidity except for the early stages. In short: the improvement of the light supply by particle retention in macrophyte stands considerably improved submersed plant development in shaded parts of the Spree during summer but was unimportant in sunny regions and during spring. This feedback effect gains importance with increasing water depth and initial particle concentration. 4.4. Compensatory effects of tree shading on epiphyton growth We found that light absorption by epiphyton at the shaded site was significantly higher than at the sunny site. Shading effects by
135
the bank tree canopy were thus not compensated by lower light absorption of the epiphytic biofilm at the shaded site. There are several possible reasons for the lack of decline in epiphyton biomass with reduced light supply. Generally, unicellular algae require less light than rooted macrophytes (SandJensen and Borum, 1991). Tuji (2000) found half of the maximum growth rate of benthic diatoms at light intensities of 5– 64 mE m2 s1 (0.25–3.2 E m2 d1 at 14 h of light per day). Rier et al. (2006) measured maximum growth of acclimated phytobenthos (mainly diatoms) at PAR > 2.5 E m2 d1. In the Spree, the upper layer of the epiphyton exposed at the shaded site in 0.5 m depth received more than 2 E m2 d1 nearly every day until mid September. In addition, the chl a to C ratio as a rough indicator for light adaptation was slightly lower at the shaded than the sunny site (Table 1). Taking these arguments together, it is highly probable that epiphyton growth was light-saturated even at the shaded site. Alternatively, high grazing pressure could explain the lacking correlation between epiphyton biomass and light (Hill, 1996). Feminella et al. (1989), Steinman (1992) and Hill et al. (1995) found biomass responses to increased light in shaded streams only after the removal of grazers. Epiphyton biomass in the Spree was significantly lower than that of downstream flushed Lake Mu¨ggelsee (Roberts et al., 2003) where predation pressure of omnivorous fish on epiphyton-grazing invertebrates is high (Okun et al., 2005). For eutrophic shallow lakes, Jones and Sayer (2003) showed that fish predation has a cascading effect on epiphytongrazing invertebrates, influencing the biomass of epiphyton and submersed plants. Direct evidence for epiphyton control by invertebrate grazing pressure in the River Spree is still lacking, so this possibility remains speculative. Epiphyton biomass was most probably not controlled by nutrient supply. Nutrient concentrations were always sufficiently high for maximum epiphyton growth (SRP > 10 mg L1, DIN > 100 mg L1, DSi > 2 mg L1, DIC > 20 mg L1). Flow favours rather than limits epiphyton accumulation and productivity (Horner et al., 1990) in the investigated velocity range of the Spree (below 40 cm s1). Therefore, epiphyton biomass was probably not controlled by high abrasive losses. This study quantified the importance of interacting effects of bank vegetation, epiphyton and suspended particles on light supply of aquatic vegetation. One of the emerging challenges is to analyse the cascading effects from fish to macroinvertebrate scrapers to epiphyton and eventually submersed macrophyte development in eutrophic lowland rivers. Acknowledgements We thank Marianne Graupe, Hanna Winkler, Barbara Meinck, Reinhard Ho¨lzel, Bernd Schu¨tze, Thomas Hintze, Christiane Herzog, Antje Lu¨der, Elke Zwirnmann, Hans-Ju¨rgen Exner and Thomas Rossoll for technical support. Jan Vermaat, Dean DeNicola, Tom Shatwell and two anonymous reviewers improved the manuscript. The study was financially supported by a grant from the Deutsche Bundesstiftung Umwelt and the Nowicki Foundation to J. Hachoł. References Anonymous, 2005. Deutsche Einheitsverfahren zur Wasser- Abwasser- und Schlamm-Untersuchung. Verlag Chemie, Weilheim. Asaeda, T., Sultana, M., Manatunge, J., Fujino, T., 2004. The effect of epiphytic algae on the growth and production of Potamogeton perfoliatus L. in two light conditions. Environ. Exp. Bot. 52, 225–238. Baker, K.S., Frouin, R., 1987. Relation between photosynthetically radiation and total insolation at the ocean surface under clear skies. Limnol. Oceanogr. 32, 1370– 1377. Bricaud, A., Stramski, D., 1990. Spectral absorption coefficients of living phytoplankton and nonalgal biogenous matter: a comparison between the Peru upwelling area and the Sargasso Sea. Limnol. Oceanogr. 35, 562–582.
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