Life form dependent impacts of macrophyte vegetation on the ratio of resuspended nutrients

water research 43 (2009) 3217–3226

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Life form dependent impacts of macrophyte vegetation on the ratio of resuspended nutrients Leena Nurminen, Jukka Horppila* Department of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, FI-00014 Helsinki, Finland

article info

abstract

Article history:

The effects of floating-leaved and submerged macrophytes on sediment resuspension and

Received 14 February 2009

on the ratio of resuspended nitrogen and phosphorus were studied by sediment traps in

Received in revised form

the Kirkkoja¨rvi basin in southern Finland. The effect of submerged macrophytes on pre-

18 April 2009

venting sediment resuspension was stronger than the effect of floating-leaved plants. On

Accepted 22 April 2009

average, among submerged plants the resuspension rate of suspended solids was 43%, and

Published online 5 May 2009

among floating-leaved plants 87% of that in the open water. The floating-leaved Nuphar lutea had a reductive effect on P resuspension but no significant effect on N resuspension.

Keywords:

The impact on P resuspension was strong, because root uptake by Nuphar lutea reduced the

Floating-leaved

P content of the sediment. N:P ratio in resuspended nutrients was 6.7 among the plants and

Life form

4.1 in the open water. Among suzbmerged plants, sediment N content was strongly

Macrophytes

increased but P content was not affected due to the pleustophytic life form of the dominant

Nutrient resuspension

plants (Ceratophyllum demersum, Ranunculus circinatus). The effect of pleustophytes on

Submerged

sediment nutrients was weak, because their nutrient uptake is mostly foliar. The N:P ratio of resuspended nutrients was 7.9 among the submerged plants and 7.0 in the open water. The results suggested that depending on the life form, macrophytes can modify the flux of N and/or P to the water column through their effects on nutrient resuspension and possibly modify phytoplankton communities via their effects on the N:P ratio. If the overall nutrient level is the most important factor for the dominance of cyanobacteria, submerged macrophytes can have stronger effects on phytoplankton community structure than floating-leaved species. If N:P ratio is of importance, the effects of floating-leaved species may be more pronounced. ª 2009 Elsevier Ltd. All rights reserved.

1.

Introduction

Aquatic macrophytes can have multiple effects on nutrient cycling in lakes. Depending, e.g., on the phase of the growing season, interactions among macrophytes, sediment and water may result in increases or decreases in the nutrient concentrations of the water (Grane´li and Solander, 1988; Stephen et al., 1997). One of the mechanisms behind the water quality effects of macrophytes is their reductive impact on sediment erosion

and resuspension rates (James and Barko, 1990). This is important, because sediment resuspension has a strong effect on nutrient cycling of lakes. In many shallow water bodies, wind-induced sediment resuspension is the main cause of internal phosphorus loading (No˜ges et al., 1998; Niemisto¨ and Horppila, 2007). Because macrophytes have a strong reductive effect on resuspension, they can substantially reduce internal phosphorus loading in lakes (Horppila and Nurminen, 2001). It has also been shown that macrophytes can promote

* Correponding author. Tel.: þ358 9 1915 8473; fax: þ358 9 1915 8257. E-mail address: [email protected] (J. Horppila). 0043-1354/$ – see front matter ª 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2009.04.041

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N retention in lakes by enhancing denitrification and by taking up nitrogen from the sediment (Christensen and Sørensen, 1986). However, the effects of macrophytes on nitrogen cycling through their effects on sediment resuspension have been only sparsely explored. The subject is of importance, since sediment resuspension often decreases the total nitrogen to total phosphorus ratio in the water because in the surface sediment the ratio is usually low, which is again attributed to intensive denitrification in the sediment (Hamilton and Mitchell, 1988; Schelske et al., 1995). Sediment resuspension may thus cause changes between phosphorus and nitrogen limitation for primary producers (Hamilton and Mitchell, 1997; Niemisto¨ et al., 2008). This may have substantial effects on algal communities, because low N:P ratios possibly favour nitrogenfixing cyanobacteria in relation to other algae (Smith, 1983; Levine and Schindler, 1999). Many studies have demonstrated that the biomass of phytoplankton among macrophyte beds is usually lower than in the open water (e.g. Søndergaard and Moss, 1998). This phenomenon has been attributed to several factors, such as shading, inhibition of sediment resuspension, competition for nutrients, refuges provided for herbivorous zooplankton, as well as allelopathic substances excreted by macrophytes (Stephen et al., 1997; Søndergaard and Moss, 1998). Some studies have indicated that in relation to other algal groups, especially the biomass of cyanobacteria is reduced among macrophyte stands (Søndergaard and Moss, 1998). The mechanisms behind this phenomenon remain unsolved (Søndergaard and Moss, 1998). This study aims to clarify, whether macrophytes have an effect on the N:P ratio of resuspended sediment, which is a possible regulatory mechanism behind the observed structuring effect of macrophyte stands on phytoplankton communities. Macrophytes can affect the nutrient concentrations in the sediment (Carignan and Kalff, 1980) and the net impact of their simultaneous effects on sediment quality and resuspension rate is not known. In this study we compare the N:P resuspension ratio among macrophyte stands and in the open water outside the stands. The regulatory mechanisms are traced by comparing submerged macrophytes having complex underwater structures but minor root system with floating-leaved species having a strong root system but very simple underwater structures. It was expected that due to their complex underwater structures, submerged species would have a stronger reductive effect on sediment resuspension rate than floatingleaved species. On the other hand, the effect of floating-leaved species on sediment nutrients and consequently on nutrient resuspension could be more remarkable than those of loosely rooted submergents. Many floating-leaved species have a high underground biomass and efficient nutrient uptake by roots.

2.

Materials and methods

2.1.

Study area

The study was performed in May–August 2000 in Kirkkoja¨rvi, which is a eutrophic separate basin of larger Lake Hiidenvesi (Fig. 1). Kirkkoja¨rvi (area 160 ha, mean depth 1.1 m) is situated in southern Finland (60 240 N, 24 180 E). The basin is

eutrophic, the average summertime total phosphorus concentration varying between 80 and 120 mg L1 and the total nitrogen concentration between 1000 and 1500 mg L1 (Nurminen and Horppila, 2002). Due to resuspended sediments and runoff from agricultural areas, the concentration of suspended solids exceeds 20 mg L1 and Secchi depth is usually below 0.5 m during the open water season (Tallberg et al., 1999). Due to the high turbidity of the water, the biomass of submerged species is quite low. Stands of species such as Ranunculus circinatus L. and Ceratophyllum demersum L. exist only in the shallow water (Nurminen, 2003). Floating-leaved species (mainly Nuphar lutea (L.) Sibth. and Sm.) form wide stands all around the basin. More detailed description on the Kirkkoja¨rvi basin and its macrophyte assemblages can be found in Nurminen et al. (2001) and Nurminen (2003).

2.2.

Data collection

The sampling station for floating-leaved species was situated in a bay in the eastern side of Kirkkoja¨rvi, the open fetch being highest (1500 m) to the west (Fig. 1). The study site for submerged species was situated in the south-western end of the basin, the highest open fetch (1800 m) being to the northeast. In both stations, sampling was conducted among the macrophytes (5–10 m from the edge) and in the adjacent open water (10–20 m from the edge). Among the stand of submerged plants, the water depth was 90 cm, and 100 cm in open water sampling site. The stand was dominated by Ceratophyllum demersum and Ranunculus circinatus, and also some Potamogeton obtusifolius Hert. and Koch existed. C. demersum and R. circinatus are pleustophytic species with a minor root system and mostly foliar nutrient uptake (Denny, 1972). In the station for floating-leaved plants Nuphar lutea dominated exclusively, and water depth was 90 cm among the stand and 110 cm in the open water. N. lutea has an extensive root and rhizome system, which constitutes to >80% of the plant biomass, and it takes nutrients primarily from the sediment (Twilley et al., 1977). The abundance of floating-leaved species was studied by measuring the changes in their stem density and the density of submerged species was estimated as per cent volume infested (PVI), calculated as the product of percentage coverage and plant height divided by water depth. Sediment resuspension rate was calculated using the method by Gasith (1975), which is applicable in shallow water bodies. The method uses the equation R¼S


fS  fT
; fR  fT

where R ¼ resuspended bottom sediment (dry weight). S ¼ entrapped settling flux (dry weight). fS ¼ organic fraction of S. fR ¼ organic fraction of R (surface sediment). fT ¼ organic fraction of seston (T) suspended in the water. The applicability of the method in the circumstances of Kirkkoja¨rvi has been tested earlier (Horppila and Nurminen, 2005). Gross sedimentation rate (S) was determined with five

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Fig. 1 – The location of the two sampling stations in Lake Hiidenvesi.

sediment traps among the plants and five traps in the adjacent open water. The traps were made from a cylindrical plastic pipe and had an inside diameter of 54 mm. The traps were lifted at 14 day intervals. The length:width ratio of the traps was 6:1 and the tops of the traps were 40 cm above the sediment. In the laboratory, the contents of the traps were dried in 105  C and weighed. The values of gross sedimentation rate (S) were corrected by subtracting the dry weight of suspended matter, contained by the water volume in each trap, from the gross dry weight per trap (Gasith, 1975). The loss on ignition (organic fraction) of the entrapped material ( fS) was determined by ignition at 550  C. On each sampling date, three replicate surface sediment samples were lifted from the macrophyte stands and the open water with a corer and analyzed for loss on ignition ( fR) and for total P concentration according to Murphy and Riley (1962) after wet combustion with sulphuric acid and hydrogen peroxide. Total N concentration of the sediment samples was measured with a LECO CHN-900 analyser. Seston samples from each zone were taken with a tube sampler, filtered through a GF/C filter and analyzed for loss on ignition ( fT) and N and P content. The rate of nutrient resuspension in each zone was calculated using the calculated resuspension rates and N and P contents of surface sediment (Horppila and Nurminen, 2001). Samples for chlorophyll a were taken with a tube sampler, filtered through Whatman GF/C filters and analysed spectrophotometrically (wavelengths 665 and 750 nm) after extraction with ethanol (Marker et al., 1980). At each station, differences in sediment and nutrient resuspension rates, nutrient and organic matter content of surface sediment and suspended seston between the vegetation zones and the open water were statistically compared with analysis of variance for repeated measurements using SAS statistical software (SAS Institute Inc., 1989). The relationship between sediment resuspension rate and the N:P resuspension ratio was studied with linear regression analysis. To improve normality, the datasets were ln(x þ 1) transformed before the analyses.

3.

Results

At both stations, macrophytes were absent when the sampling was started in May. The stem density of floating-

leaved Nuphar lutea increased steadily and reached a maximum density of 18 stems m2 on 26 July. The coverage of submerged macrophytes reached a maximum PVI of 30% in July (biomass percentages 40% Ceratophyllum demersum, 40% Ranunculus circinatus, 20% Potamogeton obtusifolius). Both macrophyte stands had a reductive effect on sediment resuspension (Figs. 2 and 3) Among floating-leaved plants, with the exception of a temporary peak in early June (67 g dw m2 d1), resuspension rate remained below 40 g dw m2 d1, while outside the plant bed it exceeded 50 g dw m2 d1 in July–August (Fig. 2). The difference between the two zones was statistically significant ( p < 0.05) (Table 1). Among submerged plants and in the adjacent open water, resuspension rate was close to 30 g dw m2 d1 in May. Among the plants, resuspension rate dropped to 2 g dw m2 d1 in August, but remained above 15 g dw m2 d1 in the open water (Fig. 3, Table 1). The rate of N resuspension among floating-leaved plants fluctuated between 140 and 380 mg m2 d1 and the rate of P resuspension between 23 and 58 mg m2 d1 (Fig. 2). The N:P ratio of resuspended sediment increased from 5.6 in May to 7.9 in August (Fig. 4). In the adjacent open water, the rate of N resuspension fluctuated between 118 and 303 mg m2 d1, which did not differ from N resuspension among the plants (Table 1). The rate of P resuspension varied between 27 and 75 mg m2 d1, which was a significantly higher rate than among the plants (Fig. 2, Table 1). The N:P ratio of resuspended nutrients in the open water was close to 4 throughout the study (Fig. 4). Among submerged plants, N resuspension rate decreased from 255 to 22 mg m2 d1 and P resuspension from 33 to 3 mg m2 d1 during the study period (Fig. 3). In the open water, resuspension rate of both nutrients was significantly higher than among the plants (Table 1). The N:P ratio of resuspended sediment fluctuated between 7.2 and 9.8 among the plants and between 5.5. and 7.6 in the open water (Fig. 4). When data from all sampling sites were pooled, the N:P ratio of resuspended nutrients decreased with increasing resuspension rate (F1,26 ¼ 17.10, R2 ¼ 0.3968, p ¼ 0.0003) (Fig. 5). When the different sampling sites were analysed separately, a significant negative dependence of resuspended N:P ratio on resuspension rate was found also in the open water adjacent to floating-leaved plants (F1,7 ¼ 6.74, R2 ¼ 0.5740, p ¼ 0.0419). Outside the submerged plant bed, on the other hand, N:P ratio

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Among floating-leaved macrophytes

80

500

70 400 60 50

300

40 200

30 20

100 10 0

0

Open water outside floating-leaved macrophytes

80

500

70 400 60 50

300

40 200

30 20

100 10

Nutrient resuspension rate (mg m-2 d-1)

Sediment resuspension rate (g dw m-2 d-1)

Nutrient resuspension rate (mg m-2 d-1)

Sediment resuspension rate (g dw m-2 d-1)

water research 43 (2009) 3217–3226

0

0 18 May1 June

1-14 June

14-28 June

28 June -12 July

Nitrogen

Phosphorus

12-26 July

26 July9 Aug.

9-23 Aug.

Sediment

Fig. 2 – The rate of sediment resuspension (line) and nutrient resuspension (columns) among floating-leaved macrophytes and in the adjacent open water during the study period. 95% confidence limits for sediment resuspension are also shown.

of resuspended nutrients increased significantly with the resuspension rate (F1,7 ¼ 8.73, R2 ¼ 0.6359, p ¼ 0.0316) (Fig. 5). Among the macrophyte stands, no significant relationship between resuspension rate and N:P ratio of resuspended nutrients was observed. In the surface sediment within the stand of floating-leaved plants, the concentration of N was 5.1 mg g1 at the start of the study and increased to 8 mg g1 in August (Table 2). Outside the plant bed, the N concentration of the sediment was significantly lower and varied from 4.7 to 5.2 mg g1 (Tables 1 and 2). The concentration of P was lower among the floatingleaved plants (1.1–1.3 mg g1) than outside the stand (0.9– 1.1 mg g1). The N:P ratio of the sediment was close to 4 among the plants throughout the study, but in the open water it fluctuated between 5 and 7.5 (Table 2). Among submerged plants, the concentration of N in the surface sediment exceeded 9 mg g1 in July and was at a significantly higher level than outside the stand, where the concentration remained below 9 mg g1 throughout the study (Tables 1 and

2). In P concentration of the sediment, no difference between the zone of submerged plants and the open water was detected (Table 1), but the P concentration fluctuated between 1.5 and 3.0 mg g1 both among the plants and in the open water (Table 2). Consequently, on most sampling dates, the N:P ratio of the sediment was higher among the plants than in the open water (Table 2). The organic matter content of the sediment was significantly higher among floating-leaved and submerged plants than in the open water (Table 1). In the sampling station for floating-leaved plants, the N content of suspended seston fluctuated between 7 and 14 mg g1 and the P content between 2 and 4 mg g1 (Table 2). No difference in the N:P ratio of suspended matter existed between the plant bed and the open water (Table 1). Among submerged plants, the N content of suspended matter was lower and P content higher than in the open water (Tables 1 and 2). N content decreased and P content increased in the course of the summer. Consequently, the N:P ratio of suspended matter decreased steeply during the study period and

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30

250

25 200 20 150 15 100 10 50

5 0

0

Open water outside submerged macrophytes

35

300

30

250

25 200 20 150 15 100 10 50

5

Nutrient resuspension rate (mg m-2 d-1)

Sediment resuspension rate (g dw m-2 d-1)

300

Nutrient resuspension rate (mg m-2 d-1)

Sediment resuspension rate (g dw m-2 d-1)

Among submerged macrophytes 35

0

0 18 May-1 June

1-14 June

14-28 June

Nitrogen

28 June 12 July Phosphorus

12-26 July

26 July-9 Aug.

9-23 Aug.

Sediment

Fig. 3 – The rate of sediment resuspension (line) and nutrient resuspension (columns) among submerged macrophytes and in the adjacent open water during the study period. 95% confidence limits for sediment resuspension are also shown.

was significantly lower among the plants than in the open water (Tables 1 and 2). The concentration of chlorophyll a was almost similar among the floating-leaved plants and the open water, and fluctuated mostly between 5 and 15 mg L1 (Table 3). Among submerged plants, chlorophyll a concentration fell to 2–3 mg L1 in July and August. In the adjacent open water, the concentration decreased in late summer as well, but did not fall below 5 mg L1 (Table 3).

4.

Discussion

4.1. General effects of different life forms on sediment resuspension Corroborating many earlier studies, macrophytes had a reductive effect on sediment resuspension rate (Barko and James, 1998; Horppila and Nurminen, 2003). As expected, the effect of submerged macrophytes was stronger than the effect of floating-leaved plants. On average, among submerged

plants the resuspension rate of suspended solids was 43%, and among floating-leaved plants 87% of that in the open water. The difference was attributed to the very simple underwater structures of N. lutea compared with the submerged species. Submerged species can effectively inhibit water currents throughout the water column, while the effect of the simple-structured N. lutea is mainly restricted to the surface (Sand-Jensen, 1998; Schulz et al., 2003). The generally higher resuspension rate at the sampling station for floatingleaved plants compared with the station for submergents was attributed to the fact that in Kirkkoja¨rvi southwesterly winds dominate and wave action is thus strongest in the eastern shores (Horppila and Nurminen, 2005). Additionally, the between-station difference in the resuspension rate and the opposite seasonal trends in the open water resuspension in the two stations were explained by the location of the macrophyte stands in relation to the dominating wind direction. In the station for submerged species, the increasing plant biomass sheltered the open water sampling location from southwesterly winds in late summer, while in the other

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Table 1 – Results from the analyses of variance for repeated measurements for the effects of macrophytes on the sediment and nutrient resuspension and surface sediment quality. Floating-leaved Vegetated vs open zone

Sediment resuspension P resuspension N resuspension Org. % in sediment P in sediment N in sediment N:P in surface sediment P in suspended seston N in suspended seston N:P in suspended seston

Time

Interaction

df

F

p

df

F

p

df

F

p

1 1 1 1 1 1 1 1 1 1

13.77 40.45 1.08 24.07 31.02 214.30 79.43 3.23 60.61 2.94

0.0008 <0.0001 0.3056 <0.0001 <0.0001 <0.0001 <0.0001 0.0938 <0.0001 0.1085

6 6 6 7 7 7 7 7 7 7

14.35 15.26 3.89 24.41 21.76 33.81 53.79 16.22 38.85 34.66

<0.0001 <0.0001 0.0072 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001

6 6 6 7 7 7 7 7 7 7

9.87 3.85 1.35 4.59 14.78 22.52 34.17 3.46 26.98 3.84

0.0002 0.0096 0.2680 <0.0001 <0.0001 <0.0001 <0.0001 0.0229 <0.0001 0.0154

Submerged Vegetated vs open zone

Sediment resuspension P resuspension N resuspension Org. % in sediment P in sediment N in sediment N:P in surface sediment P in suspended seston N in suspended seston N:P in suspended seston

F

p

df

F

p

df

F

p

1 1 1 1 1 1 1 1 1 1

10.55 219.99 129.52 131.54 2.35 53.71 30.70 26.22 56.77 69.75

0.0034 <0.0001 <0.0001 <0.0001 0.1476 <0.0001 <0.0001 0.0002 <0.0001 <0.0001

6 6 6 7 7 7 7 7 7 7

11.28 35.74 48.58 28.46 13.42 10.76 40.82 21.38 28.30 27.27

0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001

6 6 6 7 7 7 7 7 7 7

3.61 12.43 6.46 7.14 8.21 21.48 13.36 9.59 7.31 15.32

0.0108 <0.0001 0.0002 <0.0001 0.0005 <0.0001 <0.0001 0.0002 0.0008 <0.0001

Effects on the N:P ratio of resuspended sediment

Considering the whole study period, the amount of P resuspended among floating-leaved N. lutea was 62% of that in the open water (Table 4). For N, the difference between the two zones was very small (Table 4). Macrophyte impact on P resuspension was strong, because the P content of the 12

Among floating-leaved Among submerged

Outside floating-leaved Outside submerged

sediment was reduced among the plants, which together with the reduced sediment resuspension rate resulted in a strong effect. The P content of the sediment in vegetated areas may be higher or lower than in the open water area (Chambers and Prepas, 1994; Sand-Jensen, 1998), but N. lutea with a high underground biomass and nutrient uptake by roots has a strong reductive effect on sediment phosphorus. Additionally, N. lutea uptakes sediment nutrients throughout the year, which also explains the strong effect (Twilley et al., 1977). The N content of the sediment, on the other hand, was elevated among the plants, which negated the effect of the reduced sediment resuspension rate on N 12

10

Among floating-leaved Among submerged

10

8

N:P mass ratio

N:P mass ratio

Interaction

df

station there were no plants between the open water sampling location and the prevailing winds.

4.2.

Time

6 4 2

Outside floating-leaved Outside submerged

8 6 4 2 0

0 18 May-1 1- 14 June June

14-28 28 June - 12-26 26 July-9 June 12 July July Aug.

9- 23 Aug.

Fig. 4 – The mass ratio of resuspended N and P among macrophyte stands and in the adjacent open water during the study period. 95% confidence limits are also shown.

0

20

40

60

80

Resuspension rate (g dw m-2 d-1) Fig. 5 – The relationship between sediment resuspension rate and N:P mass ratio of resuspended nutrients at the different sampling sites.

Table 2 – The N and P content (mg gL1) and N:P mass ratio of surface sediment and suspended seston among the floating-leaved and submerged macrophytes and in the adjacent open water. Floating-leaved Sediment

Suspended seston

Among plants

Among plants

Open water

N

P

N:P

N

P

N:P

N

P

N:P

N

P

N:P

5.13  0.11 5.09  0.45 6.36  0.43 6.78  0.31 7.20  0.23 8.60  0.30 7.50  0.62 5.60  0.14

0.99  0.07 0.89  0.03 0.88  0.06 0.98  0.01 1.13  0.09 1.18  0.17 1.00  0.10 1.00  0.12

5.2 5.7 7.3 6.9 6.4 7.3 7.5 5.6

4.73  0.06 4.98  0.03 4.69  0.12 5.00  0.15 4.93  0.06 5.26  0.12 5.22  0.11 4.86  0.06

1.17  0.05 1.08  0.01 1.06  0.05 1.19  0.03 1.26  0.06 1.26  0.01 1.34  0.05 1.25  0.06

4.1 4.6 4.4 4.2 3.9 4.2 3.9 3.9

7.17  1.57 9.20  0.07 11.63  1.25 11.98  1.02 13.98  3.03 10.61  0.49 9.69  0.78 9.24  1.42

2.50  0.20 2.43  0.78 1.91  0.10 3.15  2.74 2.20  1.50 2.16  1.20 3.12  0.59 2.38  1.08

2.9 3.8 6.1 3.8 6.4 4.9 3.1 3.9

6.94  1.85 9.27  0.52 10.75  0.58 11.56  1.06 13.00  1.09 11.00  1.82 11.23  3.64 12.00  0.56

2.38  0.39 2.26  29 2.04  0.59 2.68  0.98 1.60  0.78 2.51  2.16 2.47  1.60 2.55  0.78

2.9 4.1 5.3 4.3 8.1 4.4 4.5 4.7

Submerged Sediment

Suspended seston

Among plants

18 May 1 Jun 14 Jun 28 Jun 12 Jul 28 Jul 9 Aug 23 Aug

Open water

Among plants

Open water

N

P

N:P

N

P

N:P

N

P

N:P

N

P

N:P

8.63  0.25 8.86  0.09 9.96  0.81 9.71  0.84 9.48  0.16 9.30  0.29 9.03  0.18 8.83  0.26

1.01  0.01 1.45  0.06 1.39  0.01 1.29  0.01 0.97  0.02 1.09  0.03 1.07  0.02 1.14  0.03

8.6 6.1 7.2 7.6 9.8 8.5 8.5 7.8

8.98  0.35 9.80  0.21 8.91  0.11 8.28  0.24 8.32  0.34 8.50  0.12 8.71  0.21 8.49  0.05

1.17  0.02 1.22  0.02 1.31  0.01 1.14  0.02 1.20  0.04 1.04  0.04 1.22  0.01 1.31  0.01

7.7 8.0 6.8 7.3 6.9 8.2 7.2 6.5

8.79  0.74 6.83  0.46 7.88  0.11 8.27  1.11 8.20  2.08 2.85  1.62 2.55  0.21 3.59  1.55

2.56  0.12 2.15  0.22 2.59  1.70 4.61  0.94 2.59  0.11 4.11  2.10 3.82  3.72 3.92  1.30

3.4 3.2 3.0 1.8 3.2 0.7 0.7 0.9

8.32  0.23 7.51  0.37 9.15  0.12 9.60  0.48 12.65  1.28 5.93  0.50 8.04  0.82 5.08  0.55

2.59  0.22 1.59  0.59 2.08  0.17 3.29  1.39 3.54  0.38 3.78  0.51 2.04  0.48 3.06  0.30

3.2 4.7 4.4 2.9 3.6 1.6 3.9 1.7

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18 May 1 Jun 14 Jun 28 Jun 12 Jul 28 Jul 9 Aug 23 Aug

Open water

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4.3. The relationship between resuspension rate and N:P ratio of resuspended matter

Table 3 – The fluctuations in the concentration of chlorophyll a (mg LL1) among floating-leaved and submerged macrophytes and in the open water. Floating-leaved

18 May 1 Jun 14 Jun 28 Jun 12 Jul 28 Jul 9 Aug 23 Aug

Submerged

Among plants

Open water

Among plants

Open water

4 10 16 12 12 13 11 11

3 11 14 13 11 12 13 18

12 6 10 6 3 3 3 2

12 6 11 10 5 6 5 6

resuspension. This again was understandable, because N in sediment is usually positively correlated with sediment organic matter and consequently also on macrophyte biomass (Sand-Jensen, 1998; Squires and Lesack, 2003). Additionally, roots are the main P uptake system for aquatic macrophytes, whereas in N uptake the role of roots is less dominant (Chambers et al., 1989). Due to the differential effects of plants on sediment N and P, N:P resuspension ratio was considerably higher among floating-leaved plants compared with areas devoid of plants. Considering the whole study period, N:P ratio in resuspended nutrients was 6.7 among the plants and 4.1 in the open water. In the N:P ratio of suspended matter, no difference between the stand of floating-leaved plants and open water existed, which was attributed to effective water exchange between the plant bed and the open water. Macrophytes with streamline underwater morphology allow water easily to pass through the vegetation (Sand-Jensen, 1998). Among submerged plants, sediment N content was increased but P content was not decreased, as expected due to the pleustophytic life form of the dominant plants. Nutrient uptake by pleustophytes is almost entirely foliar, although some nutrients may be absorbed from the sediment by the anchoring roots (Denny, 1972). Considering the whole study period, the N:P ratio of resuspended matter was 7.9 among the plants and 7.0 in the open water (Table 4). Seston quality among submerged plants was different to that in the open water, which was attributed to the effective water column coverage by the plants. Macrophyte species with complex underwater structures have high resistance against water flow (Sand-Jensen, 1998). The lower N:P ratio of suspended matter among the vegetation was due to the lower phytoplankton biomass among plants.

When the data from all sampling sites were pooled, the ratio of resuspended nutrients decreased with increasing resuspension rate. This was intelligible, because compared with inorganic sediment, highly organic sediment with a high N content has a low critical shear stress (Weyhenmeyer, 1998). Thus, the stronger the rate of sediment resuspension, the lower the organic content and the N:P ratio of the surface sediment. Accordingly, sediment N:P ratio was highest among submerged plants due to the low resuspension rate which allowed a high organic content of the sediment. When the different sampling sites were treated separately, the negative dependence of resuspended N:P ratio on resuspension rate was observed only in the open water outside floating-leaved plants, where variation in resuspension rate was high enough and variation in sediment quality low enough to result in a significant relationship. Outside submerged plants an opposite trend was observed, the N:P ratio of resuspended matter increasing together with the resuspension rate. This was due to the combination of moderate resuspension rate and high organic content of the sediment. The high organic content of the sediment revealed that water currents were not strong enough to cause significant erosion of sediment away from the sampling site during the study period. Moderate currents just recycled the organic material between the bottom and the water column at the same location, resulting in a positive dependence between resuspension rate and resuspended N:P ratio. Among the plants, resuspension rate was too low to affect the quality of resuspended matter.

4.4. Other macrophyte effects on nutrient recycling and implications for phytoplankton Resuspension is not the only mechanism, by which macrophytes affect the nutrient exchange between the sediment and the water column. For instance, oxygen release from roots affects the cycling of sediment P and N (e.g. Christensen and Sørensen, 1986; Grane´li and Solander, 1988). Macrophytes also excrete nutrients to the water (e.g. Grane´li and Solander, 1988 with references). The excretion rate by healthy shoots during the growing season is, however, usually insignificant (Smith and Adams, 1986). In all, the effects of macrophytes on the diffusion of soluble nutrients at the sediment-water interface are equivocal (e.g. Stephen et al., 1997). The effects of resuspended nutrients on phytoplankton growth depend on the release of dissolved nutrients from the resuspended particles, and that this aspect was not included in the present study.

Table 4 – The amount of nitrogen and phosphorus (mg mL2) resuspended during the 97 days study period among macrophyte stands and in the adjacent open water. Floating-leaved

N resuspension P resuspension

Submerged

Among plants

Open water

Among plants

Open water

22.8 3.4

22.2 5.4

11.1 1.4

17.6 2.5

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Depending on their P saturation level, resuspended particles can, for instance, either adsorb phosphorus from the water or release it (Søndergaard et al., 1992; Horppila and Nurminen, 2001). The importance of shallow water resuspension lies on the fact that it brings sedimentary nutrients back to the productive layers, where nutrients can be released in certain conditions (e.g. high pH, Koski-Va¨ha¨la¨ and Hartikainen, 2001). In eutrophic conditions with high nutrient demand by primary producers, both soluble phosphorus and nitrogen are often released form resuspended particles, and resuspension thus greatly increases the possibility of increased nutrient availability for phytoplankton (Søndergaard et al., 1992; Holmroos et al., in press). The effects of water column N:P ratio on the dominance of cyanobacteria is controversial. Some studies have indicated that nitrogen-fixing cyanobacteria are favoured by low nitrogen to phosphorus ratios (Smith, 1983; Levine and Schindler, 1999), while others have suggested that cyanobacterial dominance is connected to the concentration of the limiting nutrient rather than to the nutrient ratio (Trimbee and Prepas, 1987). The present study suggested that if the overall nutrient level is more important of these two, submerged macrophytes have stronger effects on phytoplankton community structure than floating-leaved species. If the N:P ratio is of importance, the effects of floating-leaved species may be more pronounced.

5.

Conclusions

The study demonstrated that aquatic macrophytes have a strong effect on the resuspension of nitrogen and phosphorus from the sediment. The amount of sediment and nutrients resuspended is effectively reduced by pleustophytic submerged plants that have complex underwater structures. Floating-leaved plants that have simple structures in the water column, but stronger root systems and more effective P uptake from the sediment than pleustophytes, have a weaker effect on sediment resuspension rate but a strong reductive impact on the N:P ratio of the resuspended material.

Acknowledgements The study was funded by the Academy of Finland (projects 50320 and 1124206) and by Alfred Kordelin foundation. Jouko Sare´n and Raija Mastonen helped with the laboratory analyses.

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