NUTRIENT LIMITATION AND PHOSPHATE
REGENERATION IN ARTIFICIAL CUTAWAY
PEATLAND LAKES
Tara Higgins and Emer Colleran
ABSTRACT
Increasingly large areas of Ireland’s emerging cutaway peatlands are being flooded to create a linked
network of lakes and wetlands designed for conservation and amenity purposes. The current study
examined water quality in four artificial cutaway peatland lakes over three years (2001 2004), with
particular focus on nutrient dynamics and the potential for phosphate to be regenerated from the
organic phosphorus pool via biotic and abiotic processes. The cutaway lakes contrasted strongly in
both their physico-chemical characteristics, trophic statuses and limiting nutrient states. Two of the
alkaline mesotrophic study lakes were annually N-limited in summer, while the acidic eutrophic
hypertrophic study lake underwent a transition to more sustained N-limitation. Laboratory
experiments indicated a considerable potential for soluble reactive phosphorus (SRP) to be
regenerated from the dissolved organic phosphorus pool by phosphatase enzyme hydrolysis (mean
2.6mg l 1). UV-induced SRP regeneration was found to play a lesser role (mean 0.9mg l1),
particularly in the dystrophic study lake, while combined UV and enzymatic hydrolysis produced an
intermediate response (mean 2.3mg l 1). With all three mechanisms, the quantity of SRP
regenerated appeared to be independent of lake trophic status. The current data provide some
evidence that the regeneration of SRP from the large organic phosphorus pool in cutaway peatland
lakes can help maintain a constant supply of bioavailable phosphorus, potentially contributing to the
prevalence of N-limiting conditions in these systems.
Tara Higgins
(corresponding
author; e-mail:
tara.higgins@
nuigalway.ie) and
Emer Colleran,
Environmental
Microbiology
Research Unit,
Department of
Microbiology,
National University of
Ireland, Galway,
Ireland.
Received 14 February
2007. Accepted 17
July 2007. Published
3 August 2007
BIOLOGY
AND
INTRODUCTION
By 2030, over 80,000ha of industrially milled
peatland will have come out of production in
Ireland. Bord na Móna is designating half of this
for wildlife conservation and public amenity uses.
The proposals include 20,000ha of shallow lakes
and wetlands, as low-lying cutaway peatlands are
reflooded. Already, 2,000ha of experimental lakes
have been created in County Offaly, in the pilot
Lough Boora Parklands project. Some of these
lakes exhibit elevated phosphorus concentrations
and high phytoplankton production rates,
particularly in the early years after inundation
(Higgins and Colleran 2006). Indeed, high
phosphorus
concentrations
precipitated
a
transition from P-limitation to secondary Nlimitation in at least one Lough Boora Parklands
lake (Higgins et al. 2006). Researchers have
attributed the eutrophication of cutaway peatland
lakes to a variety of factors: low levels of
vegetation cover increasing the vulnerability of
cutaway lakes to phosphate runoff (Wheeler and
Shaw 1995; Higgins et al. 2006); inputs of
calcareous-rich ground or surface waters
stimulating phosphorus mineralisation in the
residual peat sediments (Roelofs 1991; Smolders
ENVIRONMENT: PROCEEDINGS
OF THE
et al. 1995; Lamers et al. 1999); a lack of
established top-down control on phytoplankton
growth by zooplankton grazers (Higgins et al.
2007). Another possibility, which the current
study will explore, is that bioavailable phosphate
can be regenerated from the ample organic
phosphorus pool in cutaway peatland lakes,
thereby maintaining a continuous supply of
phosphate to the phytoplankton.
As with most shallow, organic-rich aquatic
systems (Wetzel 1983), dissolved organic
phosphorus fractions typically constitute a high
proportion of the total phosphorus in cutaway
peatland lakes (Higgins 2005). Although these
high molecular weight compounds are generally
regarded as being refractory, studies have indicated
that organic phosphorus compounds may, in fact,
represent a significant bioavailable phosphorus
source due to their susceptibility to hydrolysis and
the consequent liberation of phosphate, more
accurately termed soluble reactive phosphorus
(SRP) (Currie and Kalff 1984; Cotner and Wetzel
1992). Two common mechanisms involved in the
regeneration of SRP from organic phosphorus are:
(i) the hydrolysis of dissolved organic phosphorus
complexes by microbially generated phosphatase
ROYAL IRISH ACADEMY, VOL. 107B, NO. 3, 147 156 (2007).
#
ROYAL IRISH ACADEMY
147
BIOLOGY
AND
ENVIRONMENT
enzymes, and (ii) the abiotic UV-induced cleavage
of humic iron phosphate complexes.
determine its significance for phosphorus supply
in cutaway peatland lakes.
PHOSPHATASE HYDROLYSIS
MATERIALS AND METHODS
SRP can be made biologically available from
dissolved organic phosphorus compounds through
the action of biologically produced extracellular
hydrolytic enzymes called phosphomonoester
hydrolases, or phosphatases (Jansson 1976;
Boavida et al. 1997). Phosphatase enzymes
catalyse the hydrolysis of the organophosphate
bonds in dissolved, high molecular weight,
organic phosphomonoesters (Healey and Hendzel
1979). The net result is the release of SRP, which is
then available for biological uptake. Phosphatase
enzymes are released extracellularly from bacteria,
phytoplankton and zooplankton (Jansson 1976;
Halemejko and Chrost 1984). Many studies have
indicated that enzymatic release of SRP from
organophosphoric compounds is triggered by the
onset of phosphorus-limiting conditions (Vrba et al.
1993), indicating the adaptive production and
secretion of phosphatase enzymes during times of
phosphate depletion.
STUDY AREA AND FIELD SAMPLING
Four artificial cutaway peatland lakes, Finnamore
(N21 20), Tumduff (N18 18), Turraun (N17 23)
and Clongawny (N07 13), were investigated.
The lakes are located in the vicinity of the Lough
Boora Parklands (7843?W 53813?N), a cutaway
rehabilitation project in mid-west County Offaly,
Ireland. The study lakes were created between 1991
and 2000 by inundating 5 60ha areas of redundant
cutaway peatland to depths of 1.5 2m (for detailed
descriptions, see Higgins and Colleran 2006). The
water bodies were monitored for a range of
physico-chemical and biological parameters
between August 2001 and September 2004, at
fortnightly intervals for the first year and monthly
thereafter. Near-surface (0.2m) water samples were
collected from two sampling sites at opposite
locations on each lake. Analyses were carried out
in triplicate on all water samples: values presented in
subsequent figures and tables are the mean of the
two sampling sites at each lake.
UV-MEDIATED PHOSPHATE RELEASE
Phosphorus binds strongly to dissolved organic
matter, particularly in the presence of high
concentrations of ferric iron, thereby restricting
access to the phosphorus by microbes and
phytoplankton. Research by Francko and Heath
(1979, 1982) demonstrated that the cleavage of
phosphorus iron humic complexes in an acid bog
lake can be catalysed by mild UV radiation, of
similar strength to that found in natural sunlight,
through the photochemical reduction of ferric iron
to its ferrous form. This process released the bound
phosphate, facilitating its utilisation by bacteria and
phytoplankton. The data presented by Francko
and Heath (1979; 1982) led to concern among
limnologists that the photo-dependent release of
SRP from complex organic compounds could serve
as a significant bioavailable phosphorus supply in
other shallow peat-based lakes. Despite numerous
subsequent studies (Francko 1986; Cotner and
Heath 1990; Kilmartin 1991; McGarrigle and
Kilmartin 1992), the complex interactions in
natural waters between solar radiation and
phosphorus, iron and humics remain obscure.
The aims of the current study were (1) to
determine the nature and extent of nutrientlimitation of phytoplankton production in a
selection of four cutaway peatland lakes, and (2)
to evaluate the potential for phosphate regeneration
from the organic phosphorus pool, via UV- and
phosphatase-induced release mechanisms, and
148
PHYSICO-CHEMICAL ANALYSIS
pH was determined on-site using a portable WTW
P4 Multiline field kit. All subsequent laboratory
analyses were commenced within four hours of
collection. Water samples were filtered by passing
them through Whatman† GF/C filters (1.2mm
nominal pore size). Dissolved colour was read
spectrophotometrically at 465nm on filtered water
samples using a Hach DR4000 UV/Vis
spectrophotometer. Alkalinity was measured in
unfiltered samples using a standard H2SO4
titration method (APHA 1998). Chlorophyll-a
was analysed spectrophotometrically, using 90%
acetone-DMSO
(1:1v/v)
extraction
after
correction for phaeophytin (Burnison 1980).
Ammonium was determined on filtered samples
according to the indophenol blue method (Chaney
and Morbach 1962). Nitrite and nitrate were
measured spectrophotometrically on filtered
samples using the respective Hach diazotization
(Method 8507: range 0 0.3mg l l1 NO2 N,
precision 90.0006mg l l1 NO2 N) and
cadmium reduction (Method 8192: range 0
0.5mg l l 1 NO3 N, precision 90.01mg l1
NO3 N) methods, involving custom-defined
low-range calibrations. The sum of nitrate, nitrite
and ammonium is hereafter reported as dissolved
inorganic nitrogen (DIN). SRP, total soluble
phosphorus (TSP) and total phosphorus (TP)
were determined using the ascorbic acid reduction
NUTRIENT
LIMITATION AND PHOSPHATE REGENERATION
Cutaway Lake Water
Samples
FILTERED
SRP
Digested
UNFILTERED
UV
radiation
Enzyme
hydrolysis
Digested
TP
TSP
P-UV
P-EH
UV
radiation
P-UVEH
*
Fig. 1 Phosphorus analysis conducted on the cutaway lake water samples. (SRPsoluble reactive phosphorus; TSP
total soluble phosphorus; TPtotal phosphorus; P-UVUV-labile phosphate; P-EHenzymatically hydrolysable
phosphate; P-UVEHcombined UV-labile/enzymatically hydrolysable phosphate).
method (Murphy and Riley 1962), involving
persulphate digestion for TP and TSP analysis.
SRP and TSP were determined on filtered samples,
while TP was determined on unfiltered samples
after correction for turbidity. Soluble organic
phosphorus (SOP) was calculated as the difference
between TSP and SRP.
PHOSPHATE REGENERATION EXPERIMENTS
Phosphate
regeneration
experiments
were
conducted on seven occasions between June 2004
and January 2005 (2 June, 30 June, 14 July, 6
August, 26 August, 28 September, 26 January).
Filtered water samples were analysed for their
response to three regeneration mechanisms: UVlabile phosphate release (P-UV), enzymatically
hydrolysable phosphate release (P-EH), and both
mechanisms combined (P-UVEH). Fig. 1 illustrates
the sequence of analyses carried out on waters
samples from the four cutaway study lakes.
P-UV release
UV-induced release of phosphate was measured
using modifications of the methods described by
Francko and Heath (1982) and Cotner and Heath
(1990). Duplicate filtered water samples from each
lake were placed in shallow, acid-washed culture
trays in which water depths were maintained at
B1.5cm to ensure full UV penetration. Trays were
exposed to UVA radiation supplied by two VilberLourmat 40W tubes (dominant wavelength 365nm)
for four hours at room temperature (178C 198C).
These sources combined delivered UVA radiation
at 0.9mW cm 2 at a distance of 30cm, roughly
equivalent to the UVA present in mild solar
radiation in north-western Europe. Equivalent
control samples were incubated in darkness for
four hours. Triplicate irradiated samples and
unirradiated controls were immediately analysed
for SRP, according to the ascorbic acid reduction
method (Murphy and Riley 1962). The difference
in SRP between the dark controls and the UVirradiated samples was considered the UV-labile
phosphorus fraction of the soluble phosphorus pool,
denoted hereafter as P-UV.
P-EH and P-UVEH release
The enzymatically hydrolysable phosphorus
fraction (P-EH) was determined on cutaway lake
samples using the method described by Chrost et al.
(1986). One-litre filtered water samples from each
lake were placed in 1-litre sterile flasks, to which
was added 10ml of 1.0M tris buffer and 50ml of
pure chloroform. Samples were shaken well to
ensure sterility and incubated at 258C for five days
to promote the action of existing extracellular
phosphatase enzymes. After incubation, each
sample was divided in two parts. Half was
analysed immediately for SRP (Murphy and Riley
1962); the difference between this value and the
SRP in the initial sample was regarded as the P-EH
concentration. According to this method, any
increase in SRP after five days of incubation in
chloroform is due to free, microbially produced
dissolved phosphohydrolases, comprising primarily
phosphatases, in the water sample (Chrost et al.
1986; Bradford and Peters 1987). The second half
of the incubated sample was UV-irradiated in the
same manner as described above for P-UV. The
difference between SRP concentrations in dark
controls and the final SRP concentration after this
149
BIOLOGY
AND
combination of chloroform treatment and UV
exposure was taken as the content of P-UVEH in
the soluble phosphorus pool.
RESULTS
The data in Table 1 show that the study lakes
contrasted in terms of both their physico-chemical
characteristics and trophic statuses. Three of the
lakes * Finnamore, Tumduff and Turraun * were
alkaline, clear- to moderately coloured lakes. Based
on levels of chlorophyll-a and total phosphorus,
Finnamore and Tumduff were categorised as
mesotrophic while Turraun was mesotrophic eutrophic. Clongawny, in contrast, was acidic and
strongly coloured. Increased phosphorus inputs to
Clongawny over the sampling period led to a surge
in phytoplankton growth, and the lake underwent a
transition from being mesotrophic in 2001 to being
hypertrophic in 2004 (Higgins et al . 2006). The
very large TP pool in Clongawny was dominated
by particulate phosphorus. Mean SRP levels in the
four lakes were low, being consistently B3mg l1.
The lakes vary in terms of their limiting-nutrient
statuses, as calculated from the ratio of dissolved
inorganic nitrogen to total phosphorus (DIN:TP),
where DIN:TP B1.3 indicates N-limitation,
DIN:TP 4 indicates P-limitation and DIN:TP
between 1.3 and 4.0 indicates co-limitation by
N and P (Axler et al . 1994). Finnamore was
Table 1
*
ENVIRONMENT
generally P-limited and Turraun, Clongawny
and Tumduff were typically N-limited, although
the latter periodically experienced times of colimitation by N and P. The DIN:TP ratio varied
seasonally in Finnamore, Tumduff and Turraun
(Fig. 2a c), reflecting marked seasonal variations in
DIN concentrations, which peaked in late winter/
early spring and decreased rapidly in summertime
(Fig. 2a c). This trend was most pronounced in
Finnamore, where winter DIN concentrations
were exceeded 4mg l 1. Clongawny exhibited a
notable decline in DIN:TP ratio from spring 2002
onwards (Fig. 3d), in concert with rising
phosphorus levels in the lake and depleted DIN
concentrations (Fig. 2d) (Higgins et al. 2006).
The results of the three phosphate regeneration
experiments are presented in Fig. 4 and Table 2.
Changes in SRP in response to the three treatments
were always B5mg l 1. Irradiation with UV light
generally produced the smallest change in SRP (/x̄
0.9mg l1) (Table 2). Mean P-UV release was
highest in Turraun and lowest in Clongawny
(1.1mg l1 and 0.6mg l1 respectively). P-UV
releases were greatest on 28 September 2004 in all
lakes (2.0 3.2mg l1). All four lakes occasionally
recorded a slight decrease in SRP after UV
irradiation. Enzymatic hydrolysis generally
produced a greater increase in SRP compared
with UV irradiation (/x̄ 2.6mg l 1). Mean P-EH
release was greatest in Tumduff (3.0mg l1) and
Physico-chemical characteristics, trophic status and limiting nutrient status of four
cutaway peatland lakes. Values shown are mean, 9 standard error for 2001 2004 (n 54).
Finnamore
Tumduff
PH
Alkalinity (mg CaCO3 l 1)
Colour (mg Pt-Co l1)
Chlorophyll-a (mg l 1)
TP (mg l1)
PP (mg l1)
SOP (mg l1)
SRP (mg l1)
DIN (mg l1)
Trophic classification1
8.1190.02
17696.83
1891
5.290.4
12.290.5
5.290.3
5.290.3
1.9090.2
1,559.99169
Mesotrophic
8.0890.02
12691.79
6993
3.390.2
15.690.5
6.090.5
8.290.4
1.5990.2
243.3949
Mesotrophic
Nutrient limiting status2
P-limited
N-limited
Turraun
8.1690.03
13692.79
4791
12.791.4
26.791.5
14.591.4
9.090.4
2.2890.2
153.0926
Mesotrophic eutrophic
N-limited
Clongawny
4.6490.04
1.690.21
15693
52.596.2
39.193.4
28.993.1
7.490.6
2.7490.3
99.2917
Eutrophic hypereutrophic
N-limited
1 Calculated from mean chlorophyll-a and total phosphorus data, according to the OECD Lake Classification Scheme
(Vollenweider and Kerekes 1982).
2 Based on DIN:TP ratios, using the criteria of Axler et al . (1994): DIN:TP B1.3 indicates N-limitation, DIN:TP 4
indicates P-limitation and DIN:TP between 1.3 and 4.0 indicates co-limitation by N and P.
TP total phosphorus
PP particulate phosphorus
SOP soluble organic phosphorus.
150
SRP soluble reactive phosphorus.
DINdissolved inorganic nitrogen.
A
5,000
4,000
75
3,000
50
2,000
25
1,000
A
600
100
µg TP I-1
µg DIN I-1
LIMITATION AND PHOSPHATE REGENERATION
DIN:TP
NUTRIENT
400
200
0
0
0
75
1,000
50
500
25
0
100
750
75
500
50
250
25
0
0
1,000
C
40
20
100
750
75
500
50
250
25
0
0
Aug- Feb- Aug- Feb- Aug- Feb- Aug01 02 02 03 03 04 04
DIN
50
60
0
µg TP I-1
D
100
0
DIN:TP
C
µg TP I-1
µg DIN I-1
1,000
B
150
DIN:TP
1,500
0
µg DIN I-1
100
60
DIN:TP
B
µg TP I-1
µg DIN I-1
2,000
D
40
20
TP
*
Fig. 2a d Concentrations of dissolved inorganic
nitrogen (DIN) and total phosphorus (TP) in (a)
Finnamore, (b) Tumduff, (c) Turraun and (d)
Clongawny, between August 2001 and September 2004.
lowest in Clongawny (2.1mg l1). P-EH increases
tended to decrease towards the end of the growing
season in Finnamore, Tumduff and Turraun.
Combining both UV and enzymatic hydrolysis
treatments in general produced slightly reduced
responses compared with enzymatic hydrolysis
alone (Fig. 4 and Table 2). P-UVEH release
supplemented SRP values by a mean of 2.3mg l1
across all lakes. The responses were very similar
between the lakes, with P-UVEH ranging from
2.0mg l1 in Clongawny to 2.4mg l1 in
Finnamore and Turraun. P-UVEH release was
consistently lower than P-EH release in the earlier
part of the growing season and in January, while
P-UVEH release equalled or exceeded P-EH
release between July and September.
There was no significant relationship between
P-UV, P-EH or P-UVEH release and the initial
0
Aug- Feb- Aug- Feb- Aug- Feb- Aug01
02
02
03
03
04
04
DIN:TP ratio
*
Fig. 3a d Temporal variations in the ratio of dissolved
inorganic nitrogen to total phosphorus (DIN:TP) in (a)
Finnamore, (b) Tumduff, (c) Turraun and (d)
Clongawny, between August 2001 and September 2004.
concentrations of total phosphorus in the four study
lakes (Table 3). However, P-EH release in
Tumduff was significantly positively related to
chlorophyll-a (pB0.02), while P-EH release in
Clongawny was significantly inversely related to
SRP (pB0.05).
DISCUSSION
During the current three-year study, primary
production was predominately limited by nitrogen
availability in three of the four cutaway peatland
151
BIOLOGY
AND
ENVIRONMENT
b. Tumduff
4.0
4.0
4.0
4.0
µg I-1
6.0
2.0
0.0
1/
26
28
/0
/0
/0
9/
05
04
04
8/
04
06
26
/0
8/
04
7/
04
/0
6/
30
/0
02
/0
26
6.0
/0
6/
05
1/
9/
04
28
/0
26
06
/0
8/
8/
04
/0
7/
04
14
/0
/0
6/
6/
30
02
04
-2.0
04
-2.0
04
0.0
c. Turraun
d. Clongawny
2.0
05
04
1/
/0
26
/0
9/
04
8/
/0
8/
26
/0
28
04
04
06
/0
7/
04
14
30
/0
6/
/0
02
P-EH
6/
04
05
-2.0
/0
1/
04
P-UV
26
8/
/0
28
/0
9/
04
04
26
/0
8/
04
06
7/
/0
14
6/
30
02
/0
6/
04
04
0.0
-2.0
/0
µg I-1
2.0
0.0
14
2.0
04
µg I-1
6.0
/0
µg I-1
a. Finnamore
6.0
P-UV/EH
*
Fig. 4 Response of cutaway peatland lakes to the P-regeneration experiments, conducted on seven occasions between
June 2004 and January 2005. Values shown are mean changes in SRP; error bars show the standard error (SE). (See Fig. 1
caption for explanations of abbreviations).
lakes. This finding is significant, lending support to
the growing view that N-limitation is
underestimated as a factor affecting phytoplankton
growth in temperate lakes worldwide (Elser et al.
1990). Phosphorus has traditionally been
considered as the primary nutrient limiting
phytoplankton growth in freshwaters (Schindler
1977). Conventional lake trophic classification
models, as a result, place primacy on phosphorus
loading (Carlson 1977; Vollenweider and Kerekes
Table 2
*
1982). Only recently has the paradigm of universal
freshwater P-limitation been challenged, with a
new understanding emerging that oscillations
between P- and N-limitation occur in many
freshwater systems. Many temperate and northern
humic lakes containing low concentrations of
DIN relative to phosphorus experience seasonal
N-limitation, or co-limitation by phosphorus and
nitrogen, as available nitrogen supplies become
depleted in summertime (Hameed et al. 1999;
Summary of phosphate release in four cutaway peatland lakes by the three Pregeneration mechanisms. Values shown are mean change, mean percentage change
and minimum/maximum change in SRP (n 7). (See Fig. 1 caption for explanation
of abbreviations).
Finnamore
Tumduff
Turraun
Clongawny
All lakes
P-UV
Mean (mg l1)
Mean % change
Minimum (mg l 1)
Maximum (mg l1)
1.0
54%
0.2
2.6
0.95
70%
0.5
2.0
1.1
68%
0.5
3.2
0.6
151%
1.2
2.0
0.9
121%
0.2
3.2
P-EH
Mean (mg l1)
Mean % change
Minimum (mg l 1)
Maximum (mg l1)
2.5
238%
1.0
3.9
3.0
321%
0.9
4.1
2.9
257%
1.9
3.6
2.1
334%
1.3
3.4
2.6
362%
0.9
4.1
P-UVEH
Mean (mg l1)
Mean % change
Minimum (mg l 1)
Maximum (mg l1)
2.4
203%
1.4
3.2
2.3
182%
1.2
2.9
2.4
179%
1.6
3.8
2.0
209%
0.9
3.1
2.3
279%
0.9
3.8
152
NUTRIENT
LIMITATION AND PHOSPHATE REGENERATION
Jansson et al. 2001; Pålsson and Granéli 2004).
This occurred in Tumduff and Turraun, which
experienced N-limitation annually from late
spring until the onset of winter between 2001 and
2004. These changes reflected the reliance of these
lakes on inorganic nitrogen supply from the
catchment. DIN levels increased in winter with
nitrate runoff from surrounding agricultural areas
and were rapidly depleted with the onset of
summer as inflows receded, evaporation rates
increased and available nitrogen stocks became
depleted by primary producers (Higgins 2005).
Winter leaching of nitrate was even greater into
Finnamore lake, causing P-limiting conditions to
prevail throughout the year. Clongawny, in
contrast, underwent a transition from earlier Plimitation to extended N-limitation from May 2002
onwards (Higgins et al . 2006). This shift was
brought about by a steep rise in phosphorus levels
in the lake, the likely source of which was
phosphate fertiliser runoff from forestry
plantations on cutaway peatlands adjacent to the
lake, as identified from spatial differences in
phosphate concentrations between sampling
stations on the lake and soil and foliar nutrient
analysis from within the coniferous forestry
plantations (F. Renou, pers. comm.). There was a
concurrent depletion of DIN by the soaring
phytoplankton population, dominated by the
minute chlorophyte species Cosmarium pygmaeum
and Chlorella spp, as chlorophyll-a reached
hypertrophic
concentrations
(Higgins
and
Colleran 2006; Higgins et al. 2006). This
development of ‘unnatural’ secondary Nlimitation is common in temperate lakes that are
artificially enriched with phosphorus (Vrede et al.
Table 3
*
1999). However, it should be emphasised that
Clongawny, the youngest of the study lakes, was
inundated less than one year prior to
commencement of the current monitoring. In
view of the considerable timescales involved in
ecosystem establishment and stabilisation, further
monitoring is required in order to clarify how the
nutrient status of Clongawny, and that of the other
cutaway lakes, will evolve.
The development of N-limitation in three of
the study sites was enhanced by the consistent or
increased availability of phosphorus in the lakes
throughout the three-year study. Phosphate
regeneration experiments indicated that phosphate
can potentially be released from the large soluble
organic phosphorus pool in cutaway lake systems by
way of both biotic and abiotic regeneration
mechanisms. Enzymatic hydrolysis (P-EH)
produced the greatest response, supplementing
SRP levels in all lake samples by 2 3mg 1
(238% 334%). This mechanism was most active
in samples from Tumduff, Turraun and Finnamore
lakes and least active in Clongawny. The detection
of particularly high P-EH and P-UVEH releases in
all lake water samples collected on 2 June 2004
mirrors the maximum early summer responses
reported in other studies worldwide (Yiyong
1996; Strojsova et al. 2003). It seems to suggest
an increased reliance on enzymatically regenerated
phosphate at the end of the spring growing season,
when ambient SRP concentrations are commonly
depleted. The only significant correlation between
phosphatase enzyme activity and chlorophyll-a
concentration was found in Tumduff water
samples (pB0.02), apparently linking phosphatase
Relationship between phosphate regeneration rates and initial concentrations of
chlorophyll-a and phosphorus in the four study lakes. Values shown are Spearman
Correlation Coefficients (rs ) for non-transformed datasets; significant inverse
relationships are indicated by a minus symbol.
Finnamore
Tumduff
Turraun
Clongawny
P-UV
Chl-a
TP
SRP
0.019 ns
0.267 ns
0.008 ns
0.071 ns
0.283 ns
0.082 ns
0.137 ns
0.250 ns
0.240 ns
0.282 ns
0.004 ns
0.006 ns
P-EH
Chl-a
TP
SRP
0.04 ns
0.025 ns
0.222 ns
0.698**
0.206 ns
0.387 ns
0.014 ns
0.259 ns
0.147 ns
0.075 ns
0.244 ns
0.516*
P-EHUV
Chl-a
TP
SRP
0.097 ns
0.015 ns
0.175 ns
0.509 ns
0.033 ns
0.250 ns
0.000 ns
0.214 ns
0.123 ns
0.222 ns
0.099 ns
0.262 ns
Chl-aChlorophyll-a
TP total phosphorus
SRP soluble reactive phosphorus
ns not significant;
*p B0.05.
**p B0.02).
153
BIOLOGY
AND
enzyme production with living phytoplankton cells
in that lake. In the other lakes, bacteria,
zooplankton or decomposing phytoplankton cells
may have been the main sources of the phosphatase
enzyme activity, rather than living phytoplankton,
but further work is needed to explore this.
The release of phosphate from dissolved
humic-iron-phosphorus complexes in response to
UV irradiation was typically small in all samples.
Mean P-UV release ranged from 0.6mg l 1 in
Clongawny to 1.0mg l1 in Finnamore. In
agreement with the findings of Francko (1986)
and McGarrigle and Kilmartin (1992), a slight net
decrease in SRP (0.2 1.2mg l1) was sometimes
observed in response to UV irradiation, suggesting
the occasional precipitation of phosphate by UV
light. The reasons governing this negative response
are unclear, although factors such as the availability
and form of iron may be important. The
particularly low UV-P releases in Clongawny lend
support to the view that UV-sensitive phosphate
release processes may be less important in acidic
environments. In low pH lakes, photoreduction
rates typically exceed oxidation rates, so that most
of the iron pool is in the ferrous form (Francko
and Heath 1982; 1983), whereas humic iron
complexes only adsorb phosphate in the oxidised
ferric state (Cotner and Heath 1990). Furthermore,
the high levels of colour in humic lakes and
consequently low penetration of solar UVA
radiation mean that actual UV-mediated
phosphate release may be lower than the values
estimated by the current experiments. On only one
occasion (28 September 2004) did P-UV equal or
exceed P-EH release. High P-UV release on this
date coincided with lowered P-EH release in
Finnamore, Tumduff and Turraun. Francko and
Heath (1979) suggested that these mechanisms may
be mutually exclusively to some degree, due to the
competitive inhibition of alkaline phosphatase
activity by P-UV. Yiyong (1996) reported similar
findings for a shallow Chinese lake.
Despite large differences in initial total
phosphorus and chlorophyll-a concentrations in
the four study sites, inter-lake variations in SRP
release by the three phosphate regeneration
mechanisms were extremely small (B1mg l1).
In contrast, other studies have reported an increase
(Wright and Reddy 2001) and a reduction
(Kilmartin 1991; McGarrigle and Kilmartin 1992;
Frost and Xenopoulos 2002) in P-UV
regeneration along a phosphorus enrichment
gradient. Contradictory findings have also been
reported for P-EH release (Gage and Gorham
1985; Hino 1988). Enzymatic phosphate
regeneration is generally triggered in response to
depletion in ambient SRP concentrations, and
alkaline phosphatase activity is understood to be
actively repressed by high SRP concentrations in a
154
ENVIRONMENT
feedback inhibition process (Cembella et al. 1984;
Chrost 1991). This does not necessarily imply that
phosphate regeneration by enzymes is relevant
only to oligotrophic lakes, however, as low SRP
concentrations commonly occur in the photic
zones of eutrophic and mesotrophic lakes during
the growing season (Wetzel 1983). The significant
(pB0.05) inverse relationship found between
initial SRP levels and P-EH release in
Clongawny seems to indicate that phosphatase
enzymes were produced adaptively in this
eutrophic hypereutrophic lake in response to
periodically depleted SRP concentrations. In this
way, the phosphatase-mediated release of SRP
from the large organic phosphorus pool in
Clongawny may prevent P-limitation from
developing in this, and potentially in other, Nlimited cutaway peatland lakes. Additional research
is needed to shed light on the underlying
mechanisms and potential biological significance
of organic phosphate regeneration in cutaway
peatland lakes. Analysis of a greater number of
study sites of varying nutrient concentrations may
also reveal a link between organic phosphate
regeneration and lake trophic status. This
information holds important practical implications
for maximising the conservation value and
biodiversity potential of existing and planned
future lakes on Ireland’s cutaway peatlands.
ACKNOWLEDGEMENTS
The authors wish to thank Bord na Móna for
funding this research. The assistance of the
Environmental Change Institute, National
University of Ireland, Galway, in facilitating the
research is also appreciated.
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