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WAT E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6

0043-1354/$ - see frodoi:10.1016/j.watres

�Corresponding autE-mail address:

journal homepage: www.elsevier.com/locate/watres

Effects of light on sediment nutrient flux and water columnnutrient stoichiometry in a shallow lake

Bryan M. Spearsa,c,�, Laurence Carvalhoa, Rupert Perkinsb, David M. Patersonc

aCentre for Ecology and Hydrology Edinburgh, Penicuik, Midlothian EH26 0QB, Scotland, UKbSchool of Earth, Ocean and Planetary Sciences, Cardiff University, Main Building, Park Place, Cardiff CF10 3YE, Wales, UKcSediment Ecology Research Group, Gatty Marine Laboratory, University of St. Andrews, Fife KY16 8LB, Scotland, UK

a r t i c l e i n f o

Article history:

Received 2 July 2007

Received in revised form

14 September 2007

Accepted 16 September 2007

Available online 21 September 2007

Keywords:

Sediment

Phosphorus

Nitrogen

Silica

Flux

Lake

Light

Water column

nt matter & 2007 Elsevie.2007.09.012

hor. Centre for Ecology anspear@ceh.ac.uk (B.M. Sp

a b s t r a c t

The effects of light and temperature on nutrient cycling (silica (Si), nitrogen (N) and

phosphorus (P)) between sediments and water in a shallow eutrophic lake (Loch Leven,

Scotland), and consequent effects on water column nutrient stoichiometry, were assessed

using a series of intact sediment core incubation experiments. Estimates of actual seasonal

dark and light P-fluxes were assessed using 24-h incubations. Sediment-P uptake was

observed in spring (7 1C) and release in autumn (12 1C) and summer (17 1C), with the highest

release rates (�17 mg PO4-P m�2 sediment surface area d�1) occurring in summer. In a

longer (21-day) experiment in which the effects of light (light (n ¼ 6) and dark (n ¼ 6)) and

temperature (five 4-day cycles to represent: 7 1C)13 1C)23 1C)13 1C)7 1C) on water

column nutrient concentrations were assessed, PO4--P, total P (TP), SiO2 and total silica (TSi)

concentrations in the water column were all significantly higher under dark conditions

(ANOVA, a ¼ 0.05). NH4-N (ammonium N) water column concentrations were observed to be

higher under dark conditions at low temperatures and higher under light conditions

following a high-temperature (23 1C) treatment. No significant light effects were observed

for water column total N (TN) concentration. Flux estimates for all nutrients measured are

given. In terms of water column nutrient stoichiometry, TN:TP ratio was significantly

higher under light conditions, TSi:TN was significantly lower under light conditions, and

TSi:TP did not vary significantly between the dark and light treatments. The main

processes acting to regulate diffusive nutrient release appeared to be photosynthetic

elevation of bottom water pH and dissolved oxygen concentration (both significantly higher

under light conditions) and direct microalgal sequestration. Thus, a feedback mechanism

exists in recovering shallow lakes where benthic microalgae can affect the stoichiometry

(to favour P/Si limitation) of the plankton, and also of the main source of nutrients back to

the sediments via the disproportionate regulation of sediment P, Si and N release.

& 2007 Elsevier Ltd. All rights reserved.

1. Introduction

Benthic microalgae exist at the interface between the

sediment and the water column and, as such, are well placed

to regulate benthic/pelagic nutrient cycling. Their ability to

r Ltd. All rights reserved.

d Hydrology Edinburgh, Pears).

perform this ecosystem function may be affected by varia-

tions in light and temperature. This includes a range of

processes linked to benthic microalgae such as the replen-

ishment of organic nutrient compounds to the sediment

(Spears et al., 2007b), direct uptake of nutrients (nitrogen

enicuik, Midlothian EH26 0QB, Scotland, UK. Tel.: +44 131 4458536.

ARTICLE IN PRESS

WA T E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6978

(N)-uptake: Axler and Reuter, 1996; Webster et al., 2003;

phosphorus (P)-uptake: Barlow-Bush et al., 2006; DeNicola

et al., 2006; silica (Si)-uptake: Del Amo and Brzezinski, 1999;

Penna et al., 2003), oxygenation of the colonisation zone and,

therefore, reduction in the release of those nutrient pools that

are redox-sensitive (Woodruff et al., 1999), and biostabilisa-

tion of the sediment surface via either alteration of the

surface structure through mat formation (Dodds, 2003) or by

the enhanced cohesion and adhesion of sediment particles

caused by the extrusion of extra-cellular polymers (Paterson,

1989; Spears et al., 2007c). Although benthic microalgae

have been observed to reduce P, N and Si release from

sediments (Jansson, 1980; Kelderman et al., 1988; Jarvie et al.,

2002), it is unclear whether this regulation is constant over a

diurnal cycle and over a temperature range and whether

nutrient-specific regulation occurs resulting in alterations in

seasonality of water column stoichiometry. Additionally, no

study has considered the effects of these processes on the

cycling of these three plant nutrients together with respect to

shifts in water column stoichiometry in relation to the

Redfield ratio (i.e. 16 Si:16 N:1P; Redfield et al., 1963). This

may be particularly important in shaping phytoplankton

communities in eutrophic shallow lakes where nutritional

sources have been altered (i.e. from the catchment to the

sediment) following a reduction in external nutrient load (Sas,

1989).

Recent long-term studies have highlighted the seasonality

of benthic/pelagic nutrient cycling and water column stoi-

chiometry in recovering shallow lakes (Søndergaard et al.,

2005; Jeppesen et al., 2005). The characteristic seasonal

dynamics in water column nutrient concentrations observed

in Loch Leven are shown (Fig. 1). The contrasting seasonality

of important plant nutrients can drive phytoplankton com-

munity succession where short-term Si- and N-limitation

events are observed in spring and late summer, respectively,

and P-limitation is common during all other periods. The

occurrence of N-limitation in late summer is driven by high-

magnitude sediment-P and Si release (main source to

recovering lakes) coupled with denitrification of NO3-N

(Søndergaard et al., 2005). Although sediment disturbance

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

0.0

0.5

1.0

1.5

2.0

2.5

2

4

6

8

10

12

14

0

1

2

3

4

5

6NO3-N

PO4-P

SiO2

NO

3-N

con

cent

ratio

n (m

g L

-1)

PO4-

P co

ncen

trat

ion

(µg

L-1

)

SiO

2 co

ncen

trat

ion

(mg

L-1

)

Fig. 1 – Average monthly water column concentrations of

PO4-P, NO3-N, and SiO2 during the recovery period in Loch

Leven. Years included in the average values are 1997, 1998,

1999 and 2001.

(e.g. bioturbation and wind mixing; Welch and Cooke, 1995)

can play an important role in the cycling of nutrients between

sediments and the water column, the processes described

above are predominantly diffusive in nature and are regulated

by temperature, sediment-P release occurring on the onset of

anoxia (high temperature) resulting from a switch in sedi-

ment energy-production from autotrophy to heterotrophy

(Bostrom et al., 1988), and denitrification from an increase

(with temperature) in denitrifying bacterial production

(Risgaard-Petersen et al., 1994). Si is released from the

sediment in late summer following the dissolution of

planktonic diatom frustules (also increases with temperature)

that accumulate during spring and summer deposition

(Bailey-Watts, 1976a, b; Gibson et al., 2000), a process that

has also been linked with bacterial mediation (Bidle et al.,

2003). N is mainly released from sediment as NH4-N, which is

efficiently converted to NO3-N via nitrification under oxyge-

nated conditions (Van Luijn et al., 1995; Beutel, 2006). All of

these processes are expected to be altered under conditions

that favour benthic microalgal photosynthesis (i.e. sufficient

light conditions); P release should be reduced via the

photosynthetic elevation of dissolved oxygen (DO) concentra-

tion and moderately elevated pH conditions (ion exchange

processes can result in sediment-P release under high pH

conditions; Bostrom et al., 1988) in the surface sediment and

direct algal uptake; Si release should be reduced via direct

algal uptake; and NH4-N release should be reduced via algal

uptake and increased nitrification via the photosynthetic

elevation of surface sediment DO concentrations.

The effects of light and temperature on benthic/pelagic

nutrient cycling were tested using a series of laboratory-based

intact sediment-core incubation experiments. Two ap-

proaches were taken: (1) seasonal estimates of ambient daily

light and dark P-flux rates were taken on three separate dates

using 24-h incubations conducted at the temperature re-

corded at the time of sampling and (2) estimates of daily

water column nutrient (PO4-P, NH4-N and SiO2) concentra-

tions and stoichiometry (total silica (TSi):total N (TN):total P

(TP)) were tracked in intact sediment cores over a 21-day

incubation period for both light and dark treatments in

which temperatures were manipulated to mimic seasonal

variations.

2. Methods

2.1. Study site

Loch Leven (Fig. 2) is a shallow lake situated in the southeast

of Scotland (latitude 561100N, longitude 31300W) with a surface

area of 13.3 km2 and a mean depth of 3.9 m. The lake has a

well-documented history of eutrophication and, in an

attempt to improve water quality, external TP load was

reduced from about 4.05 mg TP m�2 lake surface area d�1 in

1985 to 1.62 mg TP m�2 lake surface area d�1 in 1995 (Bailey-

Watts and Kirika, 1999). Although improvements in water

quality conditions have recently (i.e. post 2002) been ob-

served, significant release-sensitive sediment P pools, and

associated summer internal loading events, are still common

in the lake (Spears et al., 2006, 2007b). At the time of this

ARTICLE IN PRESS

Fig. 2 – Bathymetric map of Loch Leven including the location of the sample point (cross).

Table 1 – Summary of field observations taken on each sampling date

Date Inc. temp.(1C)

Temp.(1C)

Secchi(m)

Cond.(mS cm)

pH DO(mg L�1)

23 August 2005 17.0 17.0 1.0 224 8.5 9.9

2 November 2005 12.0 10.2 1.0 220 8.5 10.5

18 April 2006 7.0 7.6 1.1 232 8.3 11.1

Inc. temp. ¼ incubation temperature, Temp. ¼ water column temperature at the time of sampling, Secchi ¼ Secchi depth, cond. ¼ water

column conductivity, DO ¼ water column dissolved oxygen concentration.

WAT E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6 979

study, therefore, Loch Leven represented a shallow lake under

recovery from eutrophication.

2.2. Sample collection

All sediment cores were collected from the same sampling

point (Fig. 2) corresponding to the mean depth (3.9 m) of the

lake. Cores were collected from a boat using a Jenkin surface-

sediment sampler that facilitated the collection of an

undisturbed sediment–water interface (core internal dia-

meter 6.7 cm and height 50 cm) consisting of about 20 cm

sediment and 30 cm overlying water column. Cores were

transported to the laboratory within 3 h of collection. All

incubations were conducted within an environmental cham-

ber in which light and temperature were regulated.

2.3. Ambient light/dark P-flux incubations

Incubations were designed to estimate the daily dark/light P-

flux rates under ambient lake conditions. Twelve cores were

collected on three dates (23 August 2005, 2 November 2005

and 18 April 2006). Surface water column temperature, DO

concentration, conductivity and pH were measured on each

date using an underwater sensor (Hydrolab Water Quality

Monitoring System, Hydrolab Corporation, Colorado, USA)

and are summarised in Table 1. Cores were transported to the

laboratory and allowed to acclimatise for 1 h in an incubator

at temperatures similar to those observed in the lake at the

time of sampling (7 1C on 18 April 2004, 12 1C on 2 November

2005 and 17 1C on 23 August 2005). On each date, six cores

were left in the light (15mmol s�1 m�2 between 8 a.m. and 4

p.m.) and six were darkened by covering with aluminium foil

and black polyethylene bags. The light levels were chosen to

mimic those observed at about 3.5 m in Loch Leven. Cores

were continually bubbled (commenced at the beginning of the

incubation period) with air using a pump (Tetratec Whisper

AP 200, TetraWerke, Melle, Germany) producing approxi-

mately 60 bubbles/min�1 with a tubing height of 23 cm above

the sediment surface. Water (15 ml) overlying the sediment

surface (sampled from 1 cm above the sediment surface) was

collected at 3:30 p.m. on the day of sampling using a syringe

immediately after the acclimatisation period and at the end

of a 24-h incubation. The differences in the concentrations

were corrected for sediment surface area and dark and light

treatment fluxes expressed as mg PO4-P m�2 sediment surface

area d�1. Only PO4-P flux was considered in the ambient P-flux

experiments and P analysis was conducted according to

Wetzel and Likens (2000).

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5

10

15

20

25

30

trie

nt f

lux

(mg

PO

4 -

P m

-2 d

-1)

WA T E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6980

2.4. Light manipulation experiment

Cores were collected on 18 April 2006. Again six cores were

left uncovered and six were incubated in the dark. The light

levels and cycle period and the bubbling rate were identical to

the conditions described for the ambient P-flux experiments.

However, temperatures were manipulated at 4 p.m. on day 1

(initial 7 1C), day 5 (initial 13 1C), day 9 (23 1C), day 13 (final

13 1C) and day 17 (final 7 1C) in this experiment. The

temperatures were maintained for 4 days following each

change. Daily water samples (20 ml) were collected (3:30 p.m.)

from 1 cm above the sediment surface (and replaced to

surface water with 20 ml distilled water) using a syringe. TP

and PO4-P analyses were conducted, using persulphate

digestion for the former, following the acid–molybdenum-

blue colorimetric method (Wetzel and Likens, 2000). NH4-N

was analysed using the phenol–hypochlorite method (Wetzel

and Likens, 2000). TN was analysed using ion chromatogra-

phy, following a persulphate digestion. TSi (following a

Na2CO3 digestion) and silicate (SiO2) concentrations were

analysed using the acid–ammonium–molybdate method

(Golterman et al., 1978). Nutrient flux estimates were made

using the difference in water column concentrations over

each 24-h period and were standardised to sediment surface

area and overlying water column volume. pH was measured

at the end of the incubation experiment (using an HI 99121 pH

meter equipped with HI 1292D soil electrode; Hanna Instru-

ments Limited, Leighton Buzzard, Bedfordshire, UK) at 1 cm

above the sediment surface and 0.5, 1.5 and 8 cm below the

sediment surface. DO concentrations were measured at about

0.5 cm above the sediment surface at the end of the

incubation experiment using a Hach Luminescent Dissolved

Oxygen probe (Model HQ10; Hach+Lang Europe, Dusseldorf,

Germany).

As in all experimental models, intact core incubation

systems have inherent problems that complicate direct

comparisons with true lake processes. These include suffi-

cient mixing of the overlying water column and potential for

disturbance of the sediments. Visual inspection of the cores

indicated no disturbance of the sediment surface at the stated

bubbling rate and chemical analysis of the water column in a

pilot study showed efficient mixing of the overlying water

under these conditions. Closed system enclosure effects can

occur in the absence of a natural flux of organic matter to the

sediment and removal of nutrients from the overlying water

column. However, this will have larger implications for long-

term incubation studies (e.g. 21-day experiment) and is less

important in short-term studies (e.g. 24-h flux estimates). As

such, the long-term experiments reported here may be used

to assess specific uptake/release mechanisms but may not

accurately represent the variations that occurred in the lake

during the same period.

-5

0

Light Dark Light Dark Light DarkSed

imen

t nu

Temperature and light treatment

7°C 12°C 17°C

Fig. 3 – Light/dark PO4-P flux under ambient lake conditions.

Error bars represent standard error of the mean (n ¼ 6).

2.5. Statistical analyses

The overall effects of temperature and light in the seasonal

ambient P-flux incubations were assessed using two-way

analysis of variance (ANOVA; total degrees of freedom

(TDF) ¼ 35, a ¼ 0.05).

In the light manipulation experiment, repeated measures

one-way ANOVAs (TDF ¼ 251, a ¼ 0.05) were used to assess

the overall effects of light on the water column concentra-

tions of NH4-N, PO4-P, SiO2, TP, TSi and TN as well as ratios of

TN:TP, TSi:TP and TSi:TN. It was impossible to statistically

differentiate between the effects of temperature and incuba-

tion time in the 21-day incubation experiments. As a result,

visual inspection of the data was used to identify gradual

‘‘incubation effects’’ from more distinct ‘‘threshold’’ tempera-

ture effects following temperature shifts.

The effects of light on variations in pH and water column

DO concentrations at the end of the incubation experiment

were assessed using one-way ANOVA.

3. Results

3.1. Ambient light/dark P flux incubations

PO4-P flux increased significantly with temperature (po0.01)

but not with light (Fig. 3). Sediment uptake of PO4-P was

observed at 7 1C with release occurring at 12 and 17 1C.

3.2. Light manipulation experiment: water columnnutrient concentrations

The results of the repeated measures one-way ANOVA analysis

used to determine the significance of the light and dark

treatments are summarised (Table 2). The ranges of nutrient

flux estimates over the 21-day incubation period are reported

(Table 3). Light and dark water column PO4-P (Fig. 4a) and TP

(Fig. 4b) concentrations showed similar trends throughout the

incubation period remaining low until day 11, following which

a sharp increase was observed which coincided with an

increase from 13 to 23 1C to suggest more rapid temperature

effects. The trends differed from day 17, with a decrease in TP

concentration in contrast to the continued increase in PO4-P

concentration, during the same period. Concentrations of both

were significantly higher under dark conditions than light

(Table 2). NH4-N concentrations also differed significantly

ARTICLE IN PRESS

WAT E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6 981

between the light treatments, being higher under dark

conditions prior to day 10. Concentrations under light condi-

tions gradually increased from day 7, with a sharper increase

on days 12 and 13. However, NH4-N concentrations decreased

from day 12 until day 16, and appeared to be triggered by the

temperature change. TN decreased between days 1 and 8 and

did not vary significantly between light and dark treatments

with no sharp temperature effects observed. SiO2 and TSi

concentrations increased gradually throughout the incubation.

Concentrations were significantly higher under dark compared

with light conditions over the 21 days.

3.3. Light manipulation experiment: water columnnutrient stoichiometry

TN:TP ratio was significantly higher under light conditions

(Table 2). TSi:TP did not vary significantly under different light

treatments. TSi:TN was significantly higher under dark

conditions.

3.4. Light manipulation experiment: pH and dissolvedoxygen profiles

The DO concentration was significantly higher under light

conditions at the end of the incubation period (dark

Table 3 – The range of sediment flux estimates measured durintotal phosphorous (TP), PO4-P, total nitrogen (TN), ammonium

TP(mg m2 d�1)

PO4-P(mg m2 d�1)

TN(mg m2 d�1)

Light �17 to +19 �2 to +11 �59 to +42

Dark �8 to +8 �1 to +4 �34 to +52

Negative values indicate sediment uptake of nutrients from the water c

column. All flux estimates are expressed as mg m�2 sediment surface ar

Table 2 – Results of the one-way repeated measuresANOVA (a ¼ 0.05) analysis used to assess the significanceof the difference between water column nutrient con-centrations (NH4-N (lg L�1), TN (mg L�1), PO4-P (lg L�1), TP(lg L�1), TSi (mg L�1), SiO2 (mg L�1)) and stoichiometry(TN:TP, TSi:TP and TSi:TN) under dark and light treat-ments

Mean light Mean dark p-Value

PO4-P 24 (24) 41 (40) 0.000

TP 47 (25) 67 (42) 0.000

NH4-N 92 (63) 62 (36) 0.021

TN 0.60 (0.17) 0.57 (0.18) 0.230

SiO2 5.6 (3.8) 7.9 (5.1) 0.000

TSi 6.2 (3.3) 8.4 (4.5) 0.000

TN:TP 42 (25) 30 (19) 0.000

TSi:TP 78 (32) 81 (43) 0.613

TSi:TN 3.0 (1.8) 4.2 (2.7) 0.000

Standard deviation of the mean (n ¼ 21) is given in parenthesis.

DO ¼ 9.25 mg L�1; light DO ¼ 9.85 mg L�1; ANOVA, a ¼ 0.05,

n ¼ 6). pH conditions (Fig. 5) were significantly higher under

light conditions at 1 cm above and 0.5 cm below the sediment

surface but no difference was observed at 1.5 and 8 cm below

the sediment surface (ANOVA; a ¼ 0.05).

4. Discussion

4.1. Ambient P-flux estimates

Estimates of P-flux rates were in agreement with a number of

recent studies in which sediment-P release has been observed

in the (warmer) summer, and sediment-P uptake observed in

the (cooler) winter months (e.g. Søndergaard et al., 2005;

Spears et al., 2007a). Other laboratory studies have found that

P release across an oxygenated sediment–water interface

becomes independent of DO concentrations at temperatures

between 17 (Kamp-Nielson, 1975) and 21 1C (Holdren and

Armstrong, 1980). This would suggest that sediment oxygen

demand exceeds sediment oxygen production at these

temperatures, creating zones of anoxia under which redox-

sensitive P complexes can be reduced and PO4-P released

from the sediment. However, no significant difference was

observed between light and dark ambient P-fluxes. This can

be explained by (1) low initial benthic algal biomass or (2) the

fact that 24 h is insufficient time for DO shifts to occur.

The low secchi depth (�1 m on each date) observed on each of

the three sampling dates indicated low light conditions at the

sediment surface (�3.5 m below the water surface) and,

therefore, it is likely there was a low initial biomass of

benthic microalgae (not measured in this study). In a previous

study, the highest epipelic biomass was observed to occur in

December/January (i.e. during clearer water periods) in Loch

Leven.

The measured release rates (Table 3) are comparatively low

for eutrophic sediments with similar estimates of ambient P

release ranging from 10 to 278 mg P m�2 sediment surface

area d�1 (Penn et al., 2000; Phillips et al., 1994, respectively)

compared with the light P-flux at 17 1C in Loch Leven, using

the same incubation techniques, estimated at 24 mg P m�2

sediment surface area d�1 (Spears et al., 2007b). Sediment-P

uptake has been observed in other studies and is generally

higher under aerated conditions (e.g. �0.22 mg m�2 d�1 in

Lake Cataouatche; Miao et al., 2006). The observed P uptake

into the sediments and the comparatively low release rates,

even under elevated temperatures, suggest that internal

nutrient cycling within Loch Leven has been reduced in

g the 21-day light manipulation incubation experiment fornitrogen (NH4-N), total silica (TSi) and silicate (SiO2)

NH4-N(mg m2 d�1)

TSi(mg m2 d�1)

SiO2

(mg m2 d�1)

�8 to +7 �189 to +887 �120 to +1126

�25 to +22 �260 to +842 �101 to +777

olumn and positive values represent sediment release to the water

ea day�1.

ARTICLE IN PRESS

0

50

100

150

200

250

300

350

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

0

50

100

150

200

250

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

0

20

40

60

80

100

120

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

DarkLight

7°C

7°C 13°C 23°C 13°C 7°C

7°C 13°C 23°C 13°C 7°C

7°C 13°C 23°C 13°C 7°C

13°C 23°C 13°C

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

TN

Incubation day

TN

con

cent

rati

on(m

g L

-1)

NH

4-N

con

cent

rati

on

(µg

L-1

)T

P c

once

ntra

tion

(µg

L-1

)P

O4-

P c

once

ntra

tion

(µg

L-1

)

TP

NH4-N

PO4-P 7°C

0

2

4

6

8

10

12

14

167°C 13°C 7°C13°C 23°C

7°C 13°C 7°C13°C 23°C

0

2

4

6

8

10

12

14

16 TSi

Incubation day

TSi

con

cent

rati

on(m

g L

-1)

SiO

2 co

ncen

trat

ion

(mg

L-1

)

SiO2

Fig. 4 – Variation in water column nutrient concentrations (PO4-P (a), TP (b), NH4-N (c), TN (d), SiO2 (e) and TSi (f)) during the

21-day incubation experiment.

WA T E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6982

ARTICLE IN PRESS

-9

-8

-7

-6

-5

-4

-3

-2

-1

0

1

2

7 7.2 7.4 7.6 7.8 8 8.2

pH

Dis

tan

ce

fro

m s

ed

ime

nt

su

rfa

ce

(c

m)

Dark

Light

Fig. 5 – Variation in pH across the sediment–water interface

following the long-term incubation experiment.

WAT E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6 983

recent years as a result of water quality management

practices.

4.2. Light manipulation experiment: effects of light onbenthic/pelagic nutrient cycling

Light and dark NH4-N water column concentrations showed

conflicting trends throughout the incubation experiment

where concentrations under light conditions were lowest

(relative to dark conditions) between days 1 and 8, and

concentrations under dark conditions were lowest following

day 12. The former observation is in agreement with our

original hypothesis where increased nitrification (i.e. lower

NH4-N concentrations) was expected under light conditions.

The higher concentrations under dark conditions are in

agreement with a number of other studies in which NH4-N

release has been reduced by benthic microalgal production

either by direct uptake or increased nitrification through the

photosynthetic elevation of DO levels (Jansson, 1980; Ris-

gaard-Petersen et al., 1994; Axler and Reuter, 1996). The shift

in apparent impacts of light on NH4-N fluxes occurs from day

9 when the temperature was increased from 13 to 23 1C,

suggesting that at this point NH4-N release increased to the

extent of masking any ‘‘dampening’’ effects of benthic algae.

Apart from the sharp change in NH4-N concentrations under

light conditions during days 12–14, all other concentration

changes were gradual and it is, therefore, impossible to

separate temperature effects from incubation effects. TN and

NH4-N variation was not synchronous throughout the in-

cubation period presumably as a result of other nitrification/

denitrification processes involving NO3-N and N2 gas. The

observed NH4-N release rates are in agreement with a number

of other studies (reviewed by Beutel (2006)) in which flux rates

are routinely observed to be lower (or negative; Zhang et al.,

2004) under well-aerated conditions. The maximum release

values were higher under dark (comparable to eutrophic

release conditions) compared with light conditions (compar-

able to mesotrophic release conditions) (Beutel, 2006) and

were generally lower than other highly productive lakes (e.g.

52–71 mg NH4-N m2 d�1 in Lake Vechten, Netherlands (Sweerts

et al., 1991)).

SiO2 concentrations increased steadily up to day 9. The rate

of release increased markedly during days 10–13, particularly

under dark conditions and coincided with a temperature

change from 13 to 23 1C. The lack of change following day 13

may represent the onset of equilibrium between the sediment

and the water column in combination with limited seques-

tration rates of Si by benthic algae. TSi and SiO2 variation was

very similar, indicating strong dependence of TSi on sedi-

ment-derived SiO2. Flux estimates were in agreement with

estimates reported in other studies (e.g. 0.1–0.8 g SiO2 m�2 d�1

in Loch Leven (Bailey-Watts, 1976b) and 0.1 g SiO2 m�2 d�1 in

Lake Grevelingen, Netherlands (Kelderman et al., 1988)).

Water column concentrations were consistently higher under

dark conditions, indicating strong regulation of Si release by

benthic microalgae. This is likely due to direct uptake. The

regulation of sediment Si release by benthic microalgae has

also been observed by Kelderman et al. (1988) and, although

not observed in this study, sediment-Si release has been

reported to increase under high temperatures (i.e. highest

release in summer; Bailey-Watts, 1976a, b; Rippey, 1983;

Gibson et al., 2000).

The pH and DO profiles measured at the end of the 21-day

incubation experiment substantiated the hypothesis that

actively photosynthesising benthic algae alter the biogeo-

chemical dynamics of sediment N and P cycling through the

maintenance of elevated DO and/or pH conditions. Few

studies have directly assessed this phenomenon in relation

to nutrient fluxes, although the profiles observed in this

study are in agreement with those observed in others. Carlton

and Wetzel (1988) observed elevated pH conditions in the

sediment surface under light conditions with significant

decreases in pH (about 1 pH unit) observed down through

the sediment. The removal of P from the water column in

Ca–P complexes is enhanced under moderate pH conditions

(i.e. above pH 6.5–7.0: Wetzel, 2001; Otsuki and Wetzel,

1972). Therefore, under the conditions observed at the end

of the incubation experiments, one may expect release of P

from Ca–P complexes in the deeper sediment layers and

precipitation of Ca–P in the water column and surface

sediments (Ca–P makes up 9.5–20.9% sediment TP in

Loch Leven; Spears et al., 2007b). However, the observed

difference of 0.1 pH unit in this study, between dark and light

conditions, is lower than the 1 pH unit difference observed in

other studies (Dodds, 2003). DO concentrations were also

higher under light (9.85 mg L�1) when compared with

dark (9.25 mg L�1) conditions. Again, this difference is low in

comparison to other studies, for example supersaturated DO

concentrations (4150% for Phormidium/Cymbella and Ulothrix-

dominated assemblages) have been observed in the surface

layers (upper 2 mm) of dense algal mats (Dodds, 2003),

probably as a result of the low (but nevertheless realistic)

light levels used in the light manipulation experiments in

comparison to these other studies. The elevated DO concen-

trations under light conditions may indicate a decrease in the

release of P from sediment Fe–P and Mn–P complexes

(reductant-soluble P makes up 23.2–39.5% sediment TP in

Loch Leven; Spears et al., 2007b) to the overlying water

column.

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Although these experiments were aerated, the significantly

higher DO concentrations observed under light conditions

reflect the elevated DO production by benthic primary

producers under illuminated conditions. These observations

strengthen the hypothesis that benthic autotrophic production

can limit P and N release through the maintenance of elevated

DO and pH conditions. Under such conditions the likelihood of

Ca–P and Fe–P release is reduced (Bostrom et al., 1988) and the

reduction of NH4-N by microbial nitrification is facilitated

(Risgaard-Petersen et al., 1994). However, direct uptake of

nutrients by benthic microalgae must also be considered and is

likely to be a key process affecting SiO2 release from the

sediment. Additionally, in situ processes may not always be so

homogeneous, and so the actual ‘‘in-lake’’ effects may be

greater than those observed in these experiments.

4.3. Light manipulation experiment: effects of light onwater column nutrient stoichiometry

The TN:TP ratio was highest, and TSi:TN ratio lowest, under

light conditions. Thus, dependent on absolute concentra-

tions, water column N-limitation may become less likely

under light conditions. The main factors regulating this

variation are likely to be driven by benthic photosynthesis

and include elevated DO concentrations and pH conditions at

the sediment surface under light conditions regulating P

release more than N release, as discussed above. However,

benthic algal production of DO has also been linked with loss

of N from the system via elevated rates of coupled nitrifica-

tion and denitrification (Van Luijn et al., 1995).

Few other studies have assessed the effects of sediment

nutrient cycling on water column nutrient stoichiometry with

the notable exception of Levine and Schindler (1992) in which

the TN:TP ratio was observed to decrease (i.e. alleviation of

N-limitation) as a result of higher N than P release from

sediments of characteristically oligotrophic lakes. This discre-

pancy highlights the importance of past nutrient loading (and,

therefore, trophic status) to a lake with respect to the internal

cycling of nutrients. Loch Leven has been impacted by elevated

external nutrient loading (both N and P) for over 125 years

(estimated using palaeolimnological techniques; unpublished

data) and experiences large sediment-P release events as a result

of high sediment-bound P stock (Spears et al., 2007b). In compa-

rison, sediment-P uptake was observed in the lakes included in

the Levine and Schindler (1992) study throughout the year,

probably as a result of low external nutrient loading. Thus, the

regulation of sediment-P release by benthic algae in oligotrophic

lakes (i.e. low/no sediment nutrient efflux) may be dominated

by direct uptake, whereas in situations where algal nutrient

requirements are saturated (i.e. eutrophic lake sediments; high

sediment nutrient efflux) indirect regulatory mechanisms (e.g.

photosynthetic production of DO) may become more important.

Additionally, indirect effects will be more important in sedi-

ments that experience conditions of anoxia.

4.4. Wider implications of the study

The sediment nutrient release scenario presented in this

paper is representative of a shallow lake recovering from

eutrophication. Under other circumstances (i.e. different

nutrient loading history) the effects of temperature and light

may be altered, as indicated by the comparison of this study

with that of Levine and Schindler (1992). However, the

observation of disproportionate regulation of sediment nu-

trient cycling highlights an interesting feedback mechanism

by which benthic microalgae may alter the flux of nutrients to

the sediment, therefore altering the stoichiometry of the

organic matter reaching the benthos (i.e. bacterial substrate)

that, in shallow lake systems such as Loch Leven, ultimately

fuels the ecology of the plankton. Eutrophication is a very

widespread problem and the need for understanding the

processes that could enhance or speed up restoration has

never been greater, particularly given European legislation

(European Commission, Water Framework Directive) that

requires waters to achieve ‘‘good’’ ecological status by 2015.

This study provides valuable information on the role of the

sediment community in influencing the recovery period.

Improved water clarity (and resultant enhancement of

sediment light regime) will be a positive feedback on recovery

and, in general, N limitation should be reduced as water

quality improves.

5. Conclusions

Ambient P-flux estimates showed sediment P uptake in

spring and release in winter and summer (greatest release

flux), which is in agreement with the characteristic seasonal P

signal in Loch Leven. No significant differences were observed

between dark and light ambient P fluxes, probably due to a

combination of low initial benthic algal biomass and high

light attenuation on the days of sampling. However, a

significant decrease in Si and P release was observed under

light conditions in the longer incubation experiments most

probably as a result of photosynthetic maintenance of DO and

pH conditions at the sediment surface (P) and direct uptake by

algae (Si and P), altering the transport of nutrients across the

sediment–water interface. Light did not significantly alter TN

cycling. The threshold effects of light and temperature with

respect to the balance between autotrophic (benthic micro-

algal) and heterotrophic (benthic bacterial) dominance and

related alterations to nutrient cycling require further inves-

tigation.

Acknowledgements

We would like to acknowledge Jamie Montgomery and the

staff at the Loch Leven Estates for continued and uninter-

rupted support and site access and Dr. Ron Smith (CEH

Edinburgh) for statistical support. We would also like to thank

the reviewers for their helpful and constructive comments.

Bryan Spears was funded by a NERC Ph.D. studentship (NERC/

S/A/2003/11324).

R E F E R E N C E S

Axler, R.P., Reuter, J.E., 1996. Nitrate uptake by phytoplanktonand periphyton: whole-lake enrichments and mesocosm-15N

ARTICLE IN PRESS

WAT E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6 985

experiments in an oligotrophic lake. Limnol. Oceanogr. 41,659–671.

Bailey-Watts, A.E., 1976a. Planktonic diatoms and some diatom–silica relations in a shallow eutrophic Scottish loch. Fresh-water Biol. 6, 69–80.

Bailey-Watts, A.E., 1976b. Planktonic diatoms and silica in LochLeven, Kinross, Scotland: a one month silica budget. Fresh-water Biol. 6, 203–213.

Bailey-Watts, A.E., Kirika, A., 1999. Poor water quality in LochLeven (Scotland) in 1995, in spite of reduced P loading since1985: the influences of catchment management and inter-annual weather variation. Hydrobiologia 403, 135–151.

Barlow-Bush, L., Baulch, H.M., Taylor, W.D., 2006. Phosphateuptake by seston in the Grand River, southern Ontario.Aquat. Sci. 68, 1615–1621.

Bidle, K.D., Brzezinski, M.A., Long, R.A., Jones, J.L., Azam, F., 2003.Diminished efficiency in the oceanic silica pump caused bybacteria-mediated silica dissolution. Limnol. Oceanogr. 45,1855–1868.

Bostrom, B., Anderson, J.M., Fleischer, S., Jansson, M., 1988.Exchange of phosphorus across the sediment–water inter-face. Hydrobiologia 170, 229–244.

Beutel, M.C., 2006. Inhibition of ammonia release from anoxicprofundal sediments in lakes using hypolymnetic oxygena-tion. Ecol. Eng. 28, 271–279.

Carlton, R.G., Wetzel, R.G., 1988. Phosphorus flux from lakesediments: effects of epipelic algal oxygen production.Limnol. Oceanogr. 33, 562–570.

Del Amo, Y., Brzezinski, M.A., 1999. The chemical form of dis-solved Si taken up by marine diatoms. J. Phycol. 35, 1162–1170.

DeNicola, D.M., de Eyto, E., Wemaere, A., Irvine, K., 2006.Periphyton response to nutrient addition in 3 lakes ofdifferent benthic productivity. J. North Am. Benthol. Soc. 25,616–631.

Dodds, W.K., 2003. The role of periphyton in phosphorus retentionin shallow freshwater aquatic systems. J. Phycol. 39, 840–849.

Gibson, C.E., Wang, G., Foy, R.H., 2000. Silica and diatom growth inLough Neagh: the importance of internal recycling. FreshwaterBiol. 45, 285–293.

Golterman, H.S., Clymo, R.S., Olmstad, M.A.M., 1978. Methods forPhysical and Chemical Analysis of Freshwaters. Blackwell,Oxford, UK.

Holdren, G.C., Armstrong, D.E., 1980. Factors affecting phosphorusrelease from intact lake sediment cores. Environ. Sci. Technol.14, 79–87.

Jansson, M., 1980. Role of benthic algae in transport of nitrogenfrom sediment to lake water in a shallow clearwater lake.Arch. Hydrobiol. 89, 101–109.

Jarvie, H.P., Neal, C., Warwick, A., White, J., Neal, M., Wickham,H.D., Hill, L.K., Andrews, M.C., 2002. Phosphorus uptake intoalgal biofilms in a lowland chalk river. Sci. Total Environ. 282,353–373.

Jeppesen, E., Søndergaard, M., Jensen, J.P., Havens, K., Anneville,O., Carvalho, L., Coveney, M.F., Deneke, R., Dokulil, M.T., Foy, B.,Gerdeaux, D., Hampton, S.E., Hilt, S., Kangur, K., Kohler, J.,Lammens, E.H.H.R., Lauridsen, T.L., Manca, M., Miracle, M.R.,Moss, B., Noges, P., Persson, G., Phillips, G., Portielje, R., Romo,S., Schelske, C.L., Straile, D., Tatrai, I., Willen, E., Winder, M.,2005. Lake responses to reduced nutrient loading—an analysisof contemporary long-term data from 35 case studies. Fresh-water Biol. 50, 1747–1771.

Kamp-Nielson, L., 1975. A kinetic approach to the aerobicsediment–water exchange of phosphorus in Lake Esrom.Ecol. Model. 1, 153–160.

Kelderman, P., Lindeboom, H.J., Klien, J., 1988. Light dependentsediment–water exchange of dissolved reactive phosphorusand silicon in a producing microflora mat. Hydrobiologia 159,137–147.

Levine, S.N., Schindler, D.W., 1992. Modification of the N:P ratio inlakes by in situ processes. Limnol. Oceanogr. 37, 917–935.

Miao, S.Y., Delaune, R.D., Jugsujinda, A., 2006. Sediment nutrientflux in a coastal lake impacted by diverted Mississippi Riverwater. Chem. Ecol. 22, 437–449.

Otsuki, A., Wetzel, R.G., 1972. Coprecipitation of phosphate withcarbonates in a marl lake. Limnol. Oceanogr. 17, 763–766.

Paterson, D.M., 1989. Short-term changes in the erodibility ofintertidal cohesive sediments related to the migratory beha-viour of epipelic diatoms. Limnol. Oceanogr. 34, 223–234.

Penn, M.R., Auer, M.T., Doerr, S.M., Driscoll, C.T., Brookes, C.M.,Effler, S.W., 2000. Seasonality in phosphorus release rates fromthe sediments of a hypereutrophic lake under a matrix of pHand redox conditions. Can. J. Fish. Aquat. Sci. 57, 1033–1041.

Penna, A., Magnani, M., Fenoglio, I., Fubini, B., Cerrano, C.,Giovine, M., Bavestrello, G., 2003. Marine diatom growth ondifferent forms of particulate silica: evidence of cell/particleinteraction. Aquat. Microb. Ecol. 32, 299–306.

Phillips, G., Jackson, R., Bennett, C., Chilvers, A., 1994. Theimportance of sediment phosphorus release in the restora-tion of very shallow lakes (The Norfolk Broads, England) andthe implications for biomanipulation. Hydrobiologia 275/276,445–456.

Redfield, A.C., Ketchum, B.H., Richards, F.A., 1963. The influenceof organisms on the composition of seawater. In: Hill, M.N.(Ed.), The Sea 2: The Composition of Seawater. Wiley, NewYork, pp. 26–77.

Rippey, B., 1983. A laboratory study of the silicon release processfrom a lake sediment (Lough Neagh, Northern Ireland). Arch.Hydrobiol. 96, 417–433.

Risgaard-Petersen, N., Rysgaard, S., Nielsen, L.P., Revsbech, N.P.,1994. Diurnal variation of denitrification and nitrificationin sediments colonized by benthic macrophytes. Limnol.Oceanogr. 39, 573–579.

Sas, H., 1989. Lake Restoration by Reduction of Nutrient Loading.Academic Verlag Richarz.

Søndergaard, M., Jensen, J.P., Jeppesen, E., 2005. Seasonal responseof nutrients to reduced phosphorus loading in 12 Danishlakes. Freshwater Biol. 50, 1605–1615.

Spears, B.M., Carvalho, L., Perkins, R., Kirika, A., Paterson, D.M.,2006. Spatial and historical variation in sediment phosphorusfractions and mobility in a large shallow lake. Water Res. 40,383–391.

Spears, B.M., Carvalho, L., Paterson, D.M., 2007a. Phosphoruspartitioning in a shallow lake: implications for water qualitymanagement. Water Environ. J. 21, 47–53.

Spears, B.M., Carvalho, L., Perkins, R., Kirika, A., Paterson, D.M.,2007b. Sediment phosphorus cycling in a large shallow lake:spatio-temporal variation in phosphorus pools and release.Hydrobiologia 584, 37–48.

Spears, B.M., Funnell, J., Saunders, J., Paterson, D.M., 2007c. On theboundaries: sediment stability measurements across aquaticecosystems. In: Westrich, B., Fostner, U. (Eds.), SedimentDynamics and Pollutant Mobility in Rivers: An Interdisciplin-ary Approach. Springer, Germany.

Sweerts, J.-P.R.A., Bar-Gilissen, M.-J., Cornelese, A.A., Cappenberg,T.E., 1991. Oxygen-consumption processes at the profundaland littoral sediment–water interface of a small meso-eutrophic lake (Lake Vechten, The Netherlands). Limnol.Oceanogr. 36, 1124–1133.

Van Luijn, F., Van der Molen, D.T., Luttmer, W.J., Boers, P.C.M.,1995. Influence of benthic diatoms on the nutrient releasefrom sediments of shallow lakes recovering from eutrophica-tion. Water Sci. Technol. 32, 89–97.

Webster, J.R., Mulholland, P.J., Tank, J.L., Valett, H.M., Dodds, W.K.,Peterson, B.J., Bowden, W.B., Dahm, C.N., Findlay, S., Gregory,S.V., Grimm, N.B., Hamilton, S.K., Johnson, S.L., Martı, E.,Mcdowell, W.H., Meyer, J.L., Morrall, D.D., Thomas, S.A.,

ARTICLE IN PRESS

WA T E R R E S E A R C H 4 2 ( 2 0 0 8 ) 9 7 7 – 9 8 6986

Wollheim, W.M., 2003. Factors affecting ammonium uptake instreams—an inter-biome perspective. Freshwater Biol. 48,1329–1352.

Welch, E.B., Cooke, GD., 1995. Internal phosphorus loading inshallow lakes: importance and control. Lake ReservoirManage. 11, 273–281.

Wetzel, R.G., 2001. Limnology: Lake and River Ecosystems, thirded. Academic Press, San Diego, USA.

Wetzel, R.G., Likens, G.E., 2000. Limnological Analyses, third ed.Springer, New York, USA.

Woodruff, S.L., House, W.A., Callow, M.E., Leadbeater, B.S.C., 1999.The effects of biofilms on chemical processes in surficialsediments. Freshwater Biol. 41, 73–89.

Zhang, X.H., Yuan, W.Y., Zhang, G.M., Sai, N., 2004. Control ofnutrients after discharge to lakes through wastewater. WaterSci. Technol. 50, 173–178.