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Chemistry and Ecology
Vol. 22, No. 2, April 2006, 93–111
Internal eutrophication: How it works and what to do
about it – a review
A. J. P. SMOLDERS*, L. P. M. LAMERS, E. C. H. E. T. LUCASSEN,
G. VAN DER VELDE and J. G. M. ROELOFS
Department of Ecology, Institute for Water and Wetland Research, Radboud University Nijmegen,
Toernooiveld 1, 6525 ED Nijmegen, The Netherlands
(Received 18 November 2005; in final form 16 January 2006)
In the 1980s and 1990s, it became increasingly clear that changes in external nutrient loads alone
could not entirely explain the severe eutrophication of surface waters in the Netherlands. Nowadays,
‘internal eutrophication’ has become a widely accepted term in Dutch water management practice to
describe the eutrophication of an ecosystem without additional external input of nutrients (N, P, K).
This review surveys the principal mechanisms involved in this process. It also discusses possible
remedies to combat internal eutrophication.
Keywords: Alkalinity; Anaerobic decomposition; Biomanipulation; Internal eutrophication; Nitrate;
Phosphate; Sulphate
1. Introduction
In the Netherlands, the term internal eutrophication (‘interne eutrofiëring’ in Dutch) has
become popular through publications by Roelofs and co-workers since the late 1980s [1–8].
Most of these publications were written in Dutch and described the eutrophication of surface
waters in Dutch peaty lowlands as a result of changes in water quality without additional
external supply of nutrients (N, P, K). Their ideas were based on the observation that water
quality had deteriorated considerably, even in nature reserves, although in many cases no
significant increase had occurred in the external nutrient loads [1, 3, 5]. Initially, this idea
was received with great scepticism. However, as it became increasingly clear that changes
in external nutrient loads alone could not possibly explain the eutrophication of the surface
waters in the Netherlands, even in areas where external nutrient loads had been considerable,
this idea gradually became accepted during the 1990s. Nowadays, internal eutrophication has
become an accepted concept in Dutch water-management practice, as well as among fellow
scientists, who have shown increasing interest in this theme.
*Corresponding author. Email: a.smolders@science.ru.nl
Chemistry and Ecology
ISSN 0275-7540 print/ISSN 1029-0370 online © 2006 Taylor & Francis
http://www.tandf.co.uk/journals
DOI: 10.1080/02757540600579730
94 A. J. P. Smolders et al.
This review presents a brief overview of the mechanisms involved in the process called
internal eutrophication, which we define as the eutrophication of an ecosystem with-
out increased external input of nutrients (N, P, K). Possible remedies to combat internal
eutrophication will also be discussed.
2. How it works
2.1 Redox equilibria and organic-matter breakdown
Organic-matter breakdown and the phosphorus-binding capacity of soil complexesare strongly
influenced by microbial processes affecting the redox state. Redox reactions can be regarded as
reactions in which transfer of electrons takes place and are generally mediated by microbes that
derive energy from electron transfer [9]. As free electrons cannot exist in aqueous solutions,
redox reactions always consist of a sub-reaction in which electrons are mobilized, and a
sub-reaction in which electrons are consumed by an electron acceptor (oxidant).
In well-oxygenated systems, oxygen serves as the primary electron acceptor:
O2+4H++4e−−→ 2H2O.
As oxygen is thermodynamically the most favourable electron acceptor, this reaction will
prevail, and as long as oxygen is present it serves as the primary oxidant in the decay of
organic matter:
Corganic +2H2O−→ CO2+4H++4e−.
In most wetlands, however, oxygen penetration into the sediment is limited and is generally
restricted to the upper 10 mm [9,10]. Only in lakes with very low organic matter contents can
oxygen penetrate deeper. Once all oxygen has been consumed or if oxygen is absent from the
start, the decay of organic matter continues by a series of reactions that represent successively
lower redox potentials (Eh).
Once oxygen levels havebecome sufficiently depleted, nitrate is used as the terminal electron
acceptor by bacteria, if it is available:
2NO−
3+12H++10e−−→ N2+6H2O
NO−
3+9H++8e−−→ NH+
4+2H2O+OH−.
This reduction of nitrate to dinitrogen gas (denitrification) or ammonium (ammonification or
dissimilatory nitrate reduction to ammonium, DNRA) involves a multitude of electron transfer
steps [9, 11].
Alternatively, iron(hydr)oxides and sulphate can become involved at successively lower
redox potentials (Eh) [9, 10, 12]:
FeOOH +3H++e−−→ Fe2++2H2O
SO2−
4+10H++8e−−→ H2S+4H2O.
The reduction of Fe and SO2−
4leads to the formation of FeSxand may result in a strong
decrease in the P-binding capacity of the sediment, as FeSxhas fewer sorption sites for P than
iron(hydr)oxides (FeOOH) [5, 7, 13,14]. This is discussed in more detail below.
Under anaerobic conditions, the availability of these alternative electron acceptors strongly
affects the breakdown of organic matter. It should be realized that although the consumption
Internal eutrophication 95
sequence of oxidants depends largely on their relative oxidative strengths, the anaerobic respi-
ration pathways are not entirely mutually exclusive, and the different pathways normally show
considerable overlap. In general, anaerobic decomposition is complex and mediated by a con-
sortium of physiologically different micro-organisms [9, 10, 12]. Fermenting bacteria bring
about extracellular hydrolysis of high-molecular-weight polymers (polysaccharides, proteins,
etc.) and ferment the products (monomers such as sugars, amino acids, etc.) to CO2,H
2,
alcohols, acetate, and other organic acids. Acetogenic bacteria are involved in the cleavage of
alcohols and organic acids into acetate, CO2, and H2. Associated with the fermentative organ-
isms are organisms that derive energy from the products of these reactions. Consumption of
acetate, H2, and CO2generally occurs by sulphate-reducing bacteria (SRB) and methanogenic
bacteria, the latter converting CO2and acetate into methane gas. The presence of the SRB and
methanogenic bacteria is therefore essential to ensure that the end-products are consumed and
that the anaerobic decay process keeps going [10, 12]. In addition to the availability of elec-
tron acceptors, (anaerobic) decomposition is obviously strongly regulated by the availability
of degradable organic matter [15].
2.2 Role of alkalinity
Apart from the lack of alternative electron acceptors, acid or very poorly buffered conditions
favour the accumulation of peat. It is well known that decomposition of organic matter is
inhibited in acid waters compared with alkaline waters [5, 16–25]. Roelofs [5] showed that the
alkalinization of surface waters in the Dutch peaty lowlands, due to the practice of letting in
alkaline river water, was responsible for an increased mineralization of the peaty substrates.
The decomposition rate of organic matter appears to be strongly correlated with the internal pH
of the detritus, while bicarbonate neutralizes the decay-inhibiting acids [20, 26]. As a result,
the decay rate of detritus appears to be a function of the buffer capacity of the surrounding
water, rather than of pH [5, 20].
Support for this hypothesis was found in a study of 600 freshwater ecosystems in the
Netherlands by Van Katwijk and Roelofs [27]. They found that the ortho-phosphate (PO3−
4,
in this review) concentrations and the bicarbonate alkalinity in surface water and sediment
pore water solutions changed in the same direction in ordination diagrams. Smolders [28] also
found a correlation between bicarbonate alkalinity and the PO3−
4and NH+
4concentrations
in sediment pore water obtained from organic freshwater sediments in the Netherlands (see
also [29]).
The effect of alkalinity on PO3−
4availability has been confirmed by an experiment in which
the alkalinity of the water layer above an undisturbed weakly buffered peat layer was increased
stepwise (figure 1). The PO3−
4levels in the water layer gradually increased as alkalinity
rose. This increase might be attributed to an increased decay rate due to the more alkaline
conditions. Apart from enhancing organic matter breakdown, however, bicarbonate can also
mobilize PO3−
4because of the competition between HCO−
3and PO3−
4for anion adsorption
sites. Although no distinction could be made between these two mechanisms, this experi-
ment does confirm that increased bicarbonate alkalinity can greatly increase the availability
of nutrients in surface waters with organic sediments.
Alkalinity may increase in response to a change in hydrology, such as letting in alkaline
surface water, or due to increased alkalinity of the groundwater [3,5, 24, 30]. However, alka-
linity may also be generated within the system by the reduction of oxidants such as nitrate,
iron(hydr)oxides or SO2−
4. The reactions under the heading ‘redox equilibria’ show that all
reduction reactions result in a net generation of alkalinity. This process is called internal
alkalinization [5]. Internal alkalinization can be observed, for instance, at ‘De Venkoelen’,
96 A. J. P. Smolders et al.
Figure 1. Increased phosphate concentrations in the water layer as a reaction to artificially increased alkalinity
above a weakly buffered fen peat sediment derived from the ‘Venkoelen’nature reserve (see also figure 2). Alkalinity
was increased stepwise on the days marked with an arrow. The experiment was carried out in glass containers
(30 ×30 ×30 cm), with a peat layer of 10 cm and a water layer of 18cm. The containers were placed in a water bath
at a constant temperature of 17 ◦C.
a minerotrophic fen in the south of the Netherlands (figure 2), where this process occurs due to
high sulphate reduction rates in summer, resulting in increased alkalinity and decreased SO2−
4
concentration in the water layer. In winter, microbial reduction processes are greatly impaired
by low temperatures, while the system is supplied with moderately buffered, sulphate-rich
groundwater, resulting in increased SO2−
4concentrations and decreased alkalinity of the water
layer (figure 2).
2.3 Increased sulphate loads
The increased availability of sulphate in ecosystems due to anthropogenic changes has received
much attention. The SO2−
4concentrations in the River Rhine are nowadays twice those mea-
sured in 1900 [31]. In the Netherlands, water from the River Rhine is let into large areas of
the peaty lowlands to prevent desiccation in summer [1,5, 29, 30]. This is necessary because
water levels are kept artificially stable. In the past, or in more natural situations, water levels
fluctuated throughout the year, being generally high in winter and low in summer. Current
water level regimes in the Netherlands tend to be the opposite: they are kept low in winter to
enable rapid runoff of excess water from agricultural lands and relatively high and stable in
summer to provide water for growth and evapotranspiration [29]. The water of the river Rhine
is alkaline and has relatively high SO2−
4concentrations [5, 7, 30].
In addition, SO2−
4concentrations in groundwater have greatly increased over the last
decades, as a consequence of increased atmospheric sulphur (S) deposition and leaching of
SO2−
4from agricultural land. Falling water tables and infiltration of nitrate (NO−
3) from agricul-
tural land and forest soils into the groundwater also increase groundwater SO2−
4concentrations
by favouring the oxidation of FeSxin the subsoil [32, 33].
The potential role of nitrate as a SO2−
4mobilizing agent has so far been largely over-
looked. Under natural conditions, nitrate (NO−
3) concentrations in groundwater are low
(<32 µmol l−1). During the last 60 yr, however, groundwater NO−
3concentrations have greatly
increased in many parts of Europe, due to increased pollution. Excessive use of manure and
synthetic fertilizers has resulted in leaching of NO−
3from agricultural lands. In Europe, the
Internal eutrophication 97
Figure 2. Variation over time of alkalinity and sulphate concentrations in the surface water of the ‘Venkoelen’,
a minerotrophic fen lake near the city of Venlo, the Netherlands. Seasonal variation can be explained by different
groundwater discharge rates and biological sulphate reduction in summer.
largest net applications of nitrogen (N) on agricultural land occur in the Netherlands and
Belgium, with surpluses of 200 and 125 kg N ha−1yr−1, respectively [34]. In addition, leakage
of NO−
3from forest soils to the groundwater has increased as gaseous ammonia and ammo-
nium sulphate aerosols are effectively filtered by tree crowns. This causes high ammonium
(NH+
4) deposition rates, especially in pine forests, and increased NO−
3concentrations in the
groundwater, as NH+
4is rapidly nitrified in forest soils, even under acid conditions [35–37].
Once it has accumulated in groundwater, NO−
3causes chemolithotrophic oxidation of pyrite
in the subsoil [38–41]. Van Steenwijk [42], for instance, observed the presence of a pyrite con-
taining layer which coincided with the disappearance of infiltrating NO−
3and an increase in
SO2−
4concentrations in the groundwater. Hence, it can be concluded that increased leaching of
nitrate from agricultural lands and forests can result in greatly increased SO2−
4concentrations
in groundwater and, after discharge, in surface water.
2.4 Sulphate-mediated eutrophication
The increased input of SO2−
4in aquatic ecosystems can lead to great changes in anaerobic
sediments. As we have seen, SO2−
4serves as an alternative electron acceptor in reductive
sediments and stimulates the decomposition of organic matter. Sulphate reduction also results
in internal alkalinization, which further enhances decomposition. Large amounts of SO2−
4may
also cause PO3−
4release due to the competition between SO2−
4and PO3−
4for anion adsorption
sites [13, 43].
Apart from this, sulphide (produced by SO2−
4reduction) also interferes with the iron-
phosphorus cycle, by reducing iron(III)(hydr)oxides and iron(III) phosphates [10, 44–48].
Subsequently, highly insoluble FeSxis formed, reducing the availability of Fe to bind PO3−
4
and increasing PO3−
4mobility [12, 14, 46–48].
98 A. J. P. Smolders et al.
This phenomenon occurs especially in soils in which a large part of the P content is bound
to Fe. Fe-rich sediments tend to retain P that becomes available from decomposition processes
and/or external P loading (figure 3). Such sediments can become loaded with P, which in itself
should not necessarily cause any problem as long as the SO2−
4loads remain low. However,
increased SO2−
4loads can easily mobilize Fe-bound P through sulphide-induced Fe binding,
which may lead to eutrophication of such systems [7, 29,45, 49]. Prolonged high SO2−
4loads
to such sediments will ultimately result in sediments in which most of the Fe is bound to
reduced sulphur (FeSx). As a consequence, the capacity of the sediment to retain P will
greatly decrease (FeSxhas far fewer sorption sites for P), which may result in decreased
total P concentrations but also in a high mobility of P in the sediments. If SO2−
4reduction
continues, toxic concentrations of free sulphide may accumulate in the sediment pore water
and cause serious problems for rooted aquatic macrophytes by inducing sulphide toxicity and
iron deficiency [7, 14, 29, 45, 49–51].
Normally, the classic iron cycle [52, 53] can very well explain the actual release of P from
the sediment. In the oxygenated boundary layer between sediment and water layer, dissolved
Fe becomes oxidized and PO3−
4is effectively bound by iron(hydr)oxides. This mechanism
probably explains the positive relation between the P-release to the water layer and the
dissolved-P:dissolved-Fe ratios in sediment pore water described by Smolders et al. [47].
Under sulphur-rich reducing conditions, however, most Fe is present as FeSx, so this mecha-
nism may no longer function [7, 13, 47]. Furthermore, dissolved sulphide (and other reduced
compounds) consumes oxygen in the top sediment layer, thus decreasing the thickness of
the oxidized boundary layer. This may greatly boost the release of dissolved PO3−
4from the
sediment. Increased methane production rates under highly reductive conditions may further
stimulate P-release by ebullition, especially in organic sediments [5, 10]. Once the sediment
becomes weak and less structured, bottom-feeding fish species such as bream (Abramis brama)
become more abundant and may further enhance the exchange of nutrients between the sedi-
ment and the water layer [54]. Increased activity of benthivorous fish may make the sediments
more susceptible to wind- and wave-induced disturbance [55], further increasing turbidity and
the release of nutrients from the sediment.
Figure 3. Relationship between total-iron content and iron-bound P concentrations in sediments derived from
different lakes in the province of Zuid-Holland (the Netherlands). P fractionation of the sediment was carried out
according to Golterman [108] and allowed a distinction between unstable (loosely bound) P, Ca-bound P, organic P,
and Fe/Al-bound P. The numbers 1–10 represent different locations.
Internal eutrophication 99
Figure 4. Soil pore water characteristics of monoliths from a minerotrophic fen meadow (‘De Bruuk’, a nature
reserve near the village of Groesbeek, the Netherlands) during 32 weeks of waterlogging with either 0 or 2 mmoll−1
sulphate (white and black marks, respectively). The figure shows means with standard errors (n=6). See also [14].
Many experiments have confirmed that increased SO2−
4loads indeed lead to increased
nutrient availability [5, 14, 15, 25, 47–49, 56–58]. Figure 4, for instance, shows the results
of an experiment in which the SO2−
4loads of monoliths obtained from a minerotrophic fen
meadow were experimentally increased (see also [14]). A SO2−
4load of 2 mmol l−1led to a
clear increase in alkalinity as well as in the PO3−
4,S
2−, and NH+
4concentrations of the soil pore
water (figure 4). At the end of the experiment, biomass regrowth after harvesting was signifi-
cantly smaller on SO2−
4-treated soils, especially for Carex species [59], though Juncus species
appeared to be more resistant to the changes. Additional experiments confirmed that sulphide
toxicity was the main cause of the decline of Carex species in the SO2−
4treatments [59].
The decline of vegetation dominated by species such as Stratiotes aloides and Potamogeton
compressus in the Netherlands can be attributed to increased SO2−
4loads and the resulting
increase in PO3−
4and NH+
4levels in the water layer, as well as increased concentrations of S2−
in sediment pore water [28, 60, 61]. Sulphide and ammonium toxicity, iron deficiency, and
increased competition by free floating macrophyte species may occur separately but frequently
also occur simultaneously (multiple stress), resulting in a considerable decrease in vitality and
finally in the complete decline of mesotrophic vegetation types (figure 5).
Vegetation shifts in aquatic systems have also been revealed by an analysis of the extensive
database collected by De Lyon and Roelofs [62]. This database includes the weighted means of
many physico-chemical variables for most of the aquatic and semi-aquatic macrophyte species
in the Netherlands. In an analysis of this database, Smolders et al. [61] tried to establish
a relationship between the weighted means of the SO2−
4and PO3−
4concentrations in the
water layer for aquatic plants in the Netherlands. For species from very reductive sediments
(Eh <−150 mV), a very clear relationship was found between these weighted means [61].
As SO2−
4is reduced in these sediments, SO2−
4-induced eutrophication by the mechanisms
described above can occur, and higher surface water SO2−
4levels may correspondingly result
in higher PO3−
4levels.
Among the species of reductive sediments, one can distinguish a group of species of waters
with SO2−
4concentrations <0.5 mmol l−1and PO3−
4concentrations <5µmol l−1(figure 6).
100 A. J. P. Smolders et al.
Figure 5. Multiple environmental stress hypothesis explaining the decline of Stratiotes aloides in the Netherlands.
Sulphate enters via surface water,groundwater, or atmospheric deposition. The reduction of sulphate to sulphide causes
eutrophication as the sulphide interacts with P binding, and mineralization is stimulated by alkalinity generation. As
a result, the water layer becomes eutrophied, leading to the dominance of floating species and algae. Simultaneously,
sulphide and ammonium toxicity and iron deficiency may occur.
These are species such as S. aloides,Potamogeton compressus,Potamogeton acutifolius, and
Utricularia vulgaris, which were once highly characteristic of the shallow surface waters in
the minerotrophic regions of the Netherlands, and are typical species of mesotrophic waters.
Two further groups that can be distinguished (II and III in figure 6) are characteristic of waters
with higher SO2−
4(weighted average between 0.7 and 1.2 mmol l−1) and PO3−
4concentrations
(weighted average between 5 and 10 µmol l−1). These groups include species such as Spirodela
polyrhiza,Lemna trisulca, and Ceratophyllum demersum, which tend to replace S. aloides or
become co-dominant in Stratiotes vegetation that has gradually become eutrophied [30].
Species of brackish waters with reductive sediment also appear to fit very well into the
scheme shown in figure 6. These species occur in waters with naturally high SO2−
4concentra-
tions and hence also high PO3−
4concentrations. It is important to realize that species adapted
to brackish water conditions have a competitive advantage over species that are not adapted to
high salinity, and therefore probably do not suffer from competition by non-rooting freshwater
species. Compared with pristine conditions, waters with Ceratophyllum submersum,Lemna
gibba, and Azolla filiculoides also have increased SO2−
4concentrations, but the weighted aver-
age of the PO3−
4concentrations in the water layer is very high. We suggest that these species
become dominant in waters in which, owing to sediment characteristics [48], increased SO2−
4
reduction leads to very strong PO3−
4mobilization, or in waters where external PO3−
4loads play
an important role.
2.5 Role of nitrate
On agricultural lands in particular, large amounts of NO−
3may be leached from the top layer
to the deeper soil layers. In situations where agricultural lands are located on top of anaerobic
Internal eutrophication 101
Figure 6. Relationship between the weighted average of the phosphate and sulphate concentrations in the water
layer for aquatic plants preferring sediments with different reductive states (Eh).The positions of species characteristic
of reductive sediments (Eh <−150 mV) are indicated in the figure by squares (I), triangles (II), diamonds (III), and
crosses. All data are derived from [62].
peaty soils, this might lead to increased decomposition of the peat, as NO−
3functions as an alter-
native electron acceptor (oxidant). Drainage ditches in such polder areas in the Netherlands
are characterized by the presence of large amounts of organic mud which cannot be explained
by the external input via surface water inlet. The mud is very probably produced within the
systems, from the decomposition of the local peat layers. Apart from aerobic decomposition
due to falling water tables and anaerobic SO2−
4-mediated breakdown, nitrate-mediated decom-
position probably plays an important role in these agricultural systems. This will be a subject
of further research in the near future.
However, NO−
3does not necessarily enhance internal eutrophication. As NO−
3is an ener-
getically more favourable electron acceptor in anaerobic sediments than Fe and SO2−
4, high
NO−
3loads may function as a redox buffer, limiting the reduction of Fe and SO2−
4[9, 63]. In
addition, NO−
3reducing bacteria have the capacity to grow anaerobically, with Fe(II) as an
electron donor, resulting in the production of Fe(III) [64–66]. It is indeed known that NO−
3
reduction can lead to the oxidation of Fe(II) [39–41, 67,68] and metal sulphides [69–72], and
so may increase the PO3−
4-binding capacity of sediments under anaerobic conditions.
The hypothesis that NO−
3may actually prevent internal eutrophication was confirmed by
recent research in Dutch alder carr fens [33, 73]. During the last decades, alder carrs in the
Netherlands have become highly eutrophied [73, 74]. Enclosure experiments have shown that
high SO2−
4reduction rates lead to PO3−
4mobilization and subsequent eutrophication [58].
However, field observations also revealed that no eutrophication occurs if there is a constant
102 A. J. P. Smolders et al.
input of groundwater that contains not only SO2−
4but also high concentrations of NO−
3[33].
The alder carrs that were fed by groundwater with high NO−
3concentrations were characterized
by the lowest PO3−
4concentrations and the development of aquatic plants characteristic of clear
waters [33].
This role of NO−
3as a redox buffer was confirmed by subsequent laboratory experi-
ments [33], in which a continuous flow of NO−
3-rich medium led to a higher redox potential
and much lower methane concentrations in the alder carr sediment than the same medium
without NO−
3. In addition, the release of Fe and S2−, resulting from the oxidation of FeSx,
Fe2+, and S2−was much lower in sediments receiving NO−
3-rich medium than in those receiv-
ing medium without NO−
3, while the release of SO2−
4was higher as a result of nitrate-induced
oxidation of FeSx.
Based on these observations, we propose the following mechanism for the current situation
in the Netherlands. NO−
3leaching from agricultural lands and forest soils leads to increased
NO−
3concentrations in the groundwater. When NO−
3reaches FeSx-containing subsoil layers,
it may oxidize FeSx, leading to the mobilization of SO2−
4and a decrease in the NO−
3concen-
tration. The resulting NO−
3:SO2−
4ratio strongly affects the quality of groundwater-fed fens. If
SO2−
4concentrations are high, and NO−
3concentrations are low, eutrophication may occur as a
result of SO2−
4reduction-related processes such as PO3−
4mobilization and Fe immobilization
(FeSxaccumulation). However, if NO−
3concentrations are also high, SO2−
4and Fe reduc-
tion are impaired, and mobilization of PO3−
4from iron-phosphate complexes is prevented. In
addition, NO−
3may oxidize reduced Fe compounds, increasing the amount of Fe3+capable
of binding PO3−
4. Hence, NO−
3leaching into the groundwater increases the risk of eutroph-
ication of the discharge areas by mobilizing SO2−
4in FeSxcontaining aquifers. However,
if NO−
3reaches a discharge area in sufficiently high concentrations, it may prevent actual
eutrophication (at least of the directly fed parts) by functioning as a redox buffer [33].
2.6 Effects of temporary oxidation
It is well known that some aquatic macrophytes, such as isoetid species, release large amounts
of oxygen from their roots and so maintain an oxidized state in the sediments [51, 75–77].As
a consequence, PO3−
4is bound to iron(hydr)oxide and remains highly immobile [78]. Taking
away the oxygen source by experimental removal of the vegetation results in an increase
in iron and PO3−
4availability due to a large decrease in redox potential [76]. These aquatic
macrophytes may therefore lower the PO3−
4availability by maintaining Fe in an oxidized
state. They can also decrease the nitrogen (N) availability by stimulating coupled nitrification–
denitrification processes [51, 79]. In the root zones and the water layer, NH+
4is nitrified to
highly mobile NO−
3, while NO−
3diffuses to the deeper anoxic sediment where it is denitrified.
In this way, oligotrophic conditions can persist for as long as 10000 yr, e.g. in soft-water lakes.
Temporary desiccation of sediments can mimic these effects and lead to lower nutrient
concentrations, while permanent high water levels may have the opposite effect. During
desiccation, pore-water PO3−
4concentrations tend to decrease as PO3−
4binds to oxidized
Fe(III) compounds, such as iron phosphate, iron(hydr)oxide-phosphate, and humic-iron-
phosphate complexes [59, 78, 80, 81]. Nitrification is stimulated after desiccation, while
subsequent waterlogging suppresses nitrification and stimulates denitrification [14, 33].
During desiccation, bicarbonate is also consumed by the oxidation of FeSxand the absence
of alkalinity-generating processes like denitrification. This can result in more poorly buffered
conditions after rewetting and hence in a decreased decomposition of organic matter.
However, Lucassen et al. [82] found that desiccation may lead to severe acidification and
mobilization of heavy metals when the sediment S/(Ca +Mg) ratio is high (>0.7 in alder
Internal eutrophication 103
carr forest). Total Ca +Mg should be regarded as a measure of the buffer capacity due to car-
bonate dissolution and cation exchange. The solubility of PO3−
4complexes, including apatite
(Ca5(PO4)3(OH,F,Cl)), strengite (FePO4), and variscite (AlPO4), is also strongly influenced by
pH. With decreasing pH, apatite is the first to dissolve, followed by variscite and strengite [83].
Hence, the present sulphur pollution in many freshwater wetlands forms a threat not only by
inducing SO2−
4-mediated internal eutrophication, but also by increasing the sensitivity of wet-
lands to desiccation [59, 82]. The combination of increased sulphur loading and a growing
risk of the occurrence of desiccation is therefore a major cause for concern. Furthermore, the
high SO2−
4concentrations generated by desiccation and the subsequent runoff following rehy-
dration inevitably cause internal eutrophication in reduced peaty soils and sediments where
the water is discharged.
At the same time, however, temporary desiccation of the top layer of the sediment appears to
be important in preventing undesirable vegetation development in well-buffered systems such
as alder carr forests [73, 84, 85]. Oxidation of insoluble FeSxleads to mobilization of SO2−
4
and precipitation of Fe as FePO4and Fe(III) hydroxides. After reflooding, the mobile SO2−
4is
removed from the system via the flowing water layer, while oxidized Fe is gradually reduced
again, also resulting in the release of immobilized P. Hence, one would expect only a minor
effect of temporary desiccation. However, in the presence of significant amounts of insoluble
reduced Fe, such as iron sulphides (FeSx) or siderite (FeCO3), oxidation of the sediment results
in a net production of Fe(III), which greatly increases the amount of reducible oxidized Fe
in the sediment capable of binding o-PO3−
4and may thus produce a more lasting beneficial
effect of desiccation [84].
This effect is illustrated by the results of an experiment in which the effect of two water
regimes (with and without a 6 week desiccation period) were tested on two sediment types [84].
One sediment originated from a zone that is fed by SO2−
4- and Fe-rich seepage during a large
part of the year and that temporarily dries out during the summer (T-sediment). This sediment
had a relatively high reduced Fe (FeSx) content. The other sediment was derived from a for-
merly dry zone without reduced Fe (D-sediment) (figure 7) and had a low reduced Fe content.
The results showed that P release from the sediment and the concomitant development of algae
and lemnids in the water layer depend on the sediment type and the interaction between sedi-
ment type and water-table fluctuations. In the T-sediment, total P concentrations in the water
layer differed greatly between the temporary desiccation treatment and the control treatment.
Desiccation of T-sediment greatly diminished the accumulation of total P in the water layer
and the concomitant biomass production of lemnids and algae in the water layer (figure 7).
Figure 7. Total P release and development of algae +Lemna spec. biomass above two different sediments (T and
D sediment, see text) from alder carr forests in the Netherlands. Values are for a 3 month period after a 6 week
desiccation period (removal of the water layer; white bars) or a control treatment with constant flooded conditions
(black bars). The water layer of the control treatment was replaced when the sediment of the desiccation treatment
was reflooded [84].
104 A. J. P. Smolders et al.
In sediments with a high reduced iron concentration, release of P to the water layer apparently
remained low for a considerable time after desiccation and subsequent re-flooding. This can
be explained by the effect that, after desiccation and re-flooding, the same amount of P is now
immobilized by a much larger pool of oxidized iron, and it thus takes a longer time before all
iron is reduced again, and the same amount of P is mobilized.
In the D-sediment, however, temporary desiccation did not lead to significant differences
in pore water P or in (total) P concentrations in the water layer after re-flooding (figure 7).
In both treatments, the water layer was extremely eutrophied, with a very high production of
filamentous algae and lemnids. Formerly dry sediments such as the D-sediment have not been
influenced by groundwater for a long time and do not possess a reduced Fe pool, which is why
desiccation did not result in an additional increase in the reducible Fe pool [84].
Oxidation of the top layer of sediment may also be achieved by increased light levels on the
sediment surface. Figure 8 shows the effects of increased light levels on the sediment surface
on the oxygen profiles in the sediment top layer and the PO3−
4concentrations in the water layer.
The sediment used in this experiment was extremely reduced, with a high FeSxcontent and
a very low concentration of dissolved iron (figure 8). In this experiment, increased irradiance
resulted in the growth of benthic algae on the sediment surface. Oxygen produced by these
algae resulted in oxidation of the sediment top layer (figure 8) and hence in the oxidation of
iron sulphide compounds. As a result, reducible iron concentrations increased in the top layer,
and PO3−
4was bound more effectively in this layer, resulting in a decreased release of PO3−
4
to the water layer (figure 8).
Figure 8. Oxygen profiles at the water/sediment interface (A), phosphate concentrations in the water layer (B),
and iron (C) and phosphate (D) concentrations in sediment pore water of a reduced sulphur- rich sediment under dark
(black squares) and light conditions (white circles) during a 5 month experimental period. Experiments (n=3) were
carried out in glass containers (25 ×25 ×30 cm), with a 10 cm sediment layer and an 18cm water layer. Under light
conditions, benthic algae were growing on the sediment surface.
Internal eutrophication 105
3. What to do about it
3.1 How to prevent eutrophication
The release of PO3−
4from eutrophic sediments strongly depends on the redox state of the
top layer. As light may stimulate the growth of water plants and benthic algae, which may
subsequently oxidize the top layer of the sediment, turbid water results in internal eutrophi-
cation, while internal eutrophication results in turbid waters. Natural water-level fluctuations
(temporary desiccation in summer) may be a prerequisite to prevent internal eutrophication
of wetlands [73, 84, 85]. This is likely to be especially true for marshes and moorland pools.
Another advantage of the oxidation of the top layer of the sediment is the fact that many
seeds in the seed beds, which do not geminate in very reductive sediments, germinate and
colonize the bottom very quickly after a short drought [28]. Ill-considered measures to pre-
vent desiccation at any cost may have disastrous consequences for such systems [73,74].
A recent strategy to minimize the use of allochthonous water in drainage ditches involves
the application of a more natural water-table management strategy, allowing higher tables in
winter and lower tables in summer. In addition, this is expected to decrease PO3−
4concentra-
tions and stimulate germination of aquatic macrophytes. However, this strategy needs further
research. Artificial oxygenation of the water layer may also increase the redox state of the
sediment top layer and prevent the release of PO3−
4to the water column [86]. It is especially
in relatively small, shallow lakes that this might be a plausible method to combat internal
eutrophication.
3.2 Biomanipulation
Clear water is essential for the development of submerged plant communities, often dom-
inated by Characeae. This condition may be achieved via a bottom-up approach, leading
to a significant reduction in the nutrient availability, or by a more top-down approach like
biomanipulation [54, 87–90]. Biomanipulation is defined as the deliberate exploitation of
the interactions between components of the aquatic ecosystem, in order to reduce the algal
biomass [87]. The main aim is to increase zooplankton (mainly Daphnia) grazing on phyto-
plankton, thereby changing from a state of turbid water to one of clear water, even though
the nutrient concentrations remain equal [89]. To achieve this, the system has to be ‘pushed’
through the hysteresis effect that prevents an easy transition from one state to the other. Once
submerged vegetation has established, it helps to maintain the clear-water equilibrium by pro-
viding a habitat and refuge for zooplankton, preventing resuspension of sediment particles,
competing with algae for nutrients and depressing algal growth by the excretion of allelopathic
substances [89, 91].
In many shallow lakes, the desired change to clear water has been achieved by a dras-
tic reduction of the zooplanktivorous and benthivorous fish stocks [54, 87, 88, 92–94]. This
involves a reduction to 10–15kg ha−1and 15–25 kg ha−1of zooplanktivorous and benthivo-
rous fish, respectively (generally corresponding to a minimum reduction of 75%). In addition,
piscivorous fish like Esox lucius (Northern pike) and Stizostedion lucioperca (Pikeperch)
may be introduced or reintroduced. In some fens, such biomanipulation turned out to be
very effective in re-establishing underwater light conditions that are favourable to submerged
macrophytes. In others, however, the water remained turbid or became turbid again quickly
after the measures were taken, and submerged plant communities failed to develop.
In hypertrophic lakes, turbidity is the only possible stable situation. Biomanipulation will
only work after PO3−
4concentrations are reduced to a range in which two alternative stable
106 A. J. P. Smolders et al.
states are possible [89]. The actual threshold value seems to lie below about 7µmol total
Pl
−1, although shallow lakes may be clear at much higher concentrations [88, 95]. This can
be attributed to the strong influence of submerged macrophytes on water quality, as explained
earlier. Poor results with biomanipulation in fens well within the range of two alternative
stable states are often caused by insufficient reduction of the fish stock or by massive fish
remigration from small interconnected ditches or through fish exclosures [96]. In most fen
waters, the best way of fighting eutrophication seems to lie in a combination of biomanipula-
tion (top-down control) and active reduction of the influx and internal mobilization of PO3−
4
(bottom-up).
3.3 Phosphate inactivation
Phosphorus can be very effectively bound in the form of calcium phosphates. In south-west
Norway,for instance, P concentrations as high as 100 mmol g−1DW are encountered in the sed-
iments, but the lakes can still be characterized as ultra-oligotrophic, since almost all P is present
in the form of highly insoluble fluorapatite (Ca5F(PO4)3). In hard-water lakes, lime additions
have shown some potential for controlling P availability [97, 98]. Lime application may super-
saturate the water column with Ca2+, which can result in precipitation of (hydroxy)apatite and
also cause precipitation of phytoplankton. Binding P as calcium phosphate precipitation might
have great advantages, as Ca-bound P is redox-insensitive. However, compared with Fe and
Al additions, liming seems to be less effective [86], and multiple treatments may be necessary
for long-term management of phytoplankton biomass [97, 98]. In soft-water lakes with a peaty
sediment, the addition of lime to bind PO3−
4will not work, because of the strong stimulation
of P mineralization in fen peat (see above), overruling any possible effect of chemical binding
of P [5, 28, 29].
The addition of Fe or Al to sediments to bind PO3−
4(PO3−
4inactivation) has a strong de-
eutrophying effect in both lakes and fens [47, 49, 86, 98–102]. Burley et al. [86] concluded
that Fe(III) and Al addition were more effective than liming, although cost-effectiveness
considerations may make these methods less desirable [47, 98]. If there is a constant sup-
ply of SO2−
4enriched water, the response is only transient, because Fe consumption is
extremely high [47, 49, 86]. In such cases, Fe addition has proved to be too laborious
and costly to be recommended as a general and large-scale restoration measure against
eutrophication [47].
Aluminium addition has the advantage that Al-bound P is redox-insensitive and indeed
seems to be able to bind P more effectively than Fe [103]. A special problem related to
the addition of aluminium salts, however, is the fact that Al may cause toxicity symptoms,
especially in the fauna component of the system. Acidification due to Alx(OH)3forma-
tion (hydrolization) may lead to high concentrations of highly toxic inorganic monomeric
Al (Al3+) [104], while subsequent polymerization reactions (formation of Al hydroxides)
can temporarily result in an even greater toxicity [105]. Although, in well-buffered (alka-
line) lakes, such highly toxic shock events will be both local and temporary, they may
still be considered highly undesirable, especially when valuable fauna components are
present.
The presence of dense macrophyte stands may cause problems, especially when Ca, Fe, or Al
is applied directly to the water layer [102]. In cases where P is bound to the top layer following
the addition of Ca/Fe/Al, sediment P may be taken up directly from below the treated top
layer. The nutrients taken up from the sediment by these macrophytes then become available in
the water layer due to senescence and decay. Finally, Ca/Fe/Al-treated sediment may become
buried if sedimentation rates remain relatively high and so lose their effectiveness [102].
Internal eutrophication 107
3.4 Sediment removal
Dredging of PO3−
4-enriched and/or iron-depleted sediments is another option and can be
highly effective [106,107]. However, if no additional measures are taken, the effect of sed-
iment removal is also temporary. In eutrophied, poorly buffered systems, sediment removal
may lead to a strong decrease in nutrient levels in the water layer, but also to a severe decrease
in the base saturation of the sediment. As long as water rich in acid and/or ammonium
enters the system, acidification or re-acidification of these systems may occur. An adequate
additional measure to counteract re-acidification may be a controlled supply of calcareous
groundwater [106]. Problems linked with sediment removal, however, are not only the high
costs but also the fact that, according to the present environmental standards, the sediment in
many cases has to be technically classified as chemical waste because of accumulated toxic
compounds.
4. Final comments
It can be concluded that internal eutrophication may play an important role in the deterioration
of aquatic ecosystems. Increased breakdown of organic matter under anaerobic conditions due
to increased alkalinity and increased availability of oxidants (SO2−
4and possibly nitrate) play
key roles in this process. In addition, the interference of SO2−
4with the iron-phosphate cycle is
of paramount importance. The restoration of the original, semi-natural hydrology (high water
levels in winter and low water levels in summer), both at the landscape level and at the habitat
level, may reduce the negative effects or may even be a prerequisite for an acceptable water
quality. Such measures will decrease the SO2−
4and alkalinity loads of the systems and might
also increase the P-binding capacity of the sediments if temporary desiccation should occur.
Biomanipulation is a costly but potentially effective method by which an alternative stable
state can be reached, which permits clear water even while nutrient concentrations in the water
layer remain high. Treatments of whole water bodies with lime, iron, or aluminium salts have
also proved to be potentially effective. However, such measures are also costly, while the
improvement of the water quality is often transient.
More generally, it is important to realize that agriculture on peaty substrates, which is
currently being practised on a large scale in the Netherlands, is not sustainable. A complete
hydrological isolation of large areas would probably be the best way to prevent internal eutroph-
ication processes. Allowing more rain water to accumulate in the wetlands would reduce not
only the alkalinity but also the SO2−
4load. Next, old seepage systems might be restored, which
would result locally in a renewed supply of iron via the groundwater. Raising water tables
and decreasing nitrate loads from former agricultural lands could further diminish the SO2−
4
concentrations in groundwater.This might allow large marshes to start re-developing, and peat
could build up again in areas where organic soil is currently broken down rapidly. This would
diminish soil subsidence as well as net carbon losses to the atmosphere. Given the agricul-
tural functions involved, such measures would not be a feasible option at present. In the long
run, however, these alternative options might become more attractive because agriculture is
economically under great pressure, especially in the wet lowland areas.
Acknowledgements
The authors wish to thank Mr Jan Klerkx and Dr Hilde Tomassen for critically reading the
manuscript.
108 A. J. P. Smolders et al.
References
[1] F.H.J.L. Bloemendaal, J.G.M. Roelofs. Waterplanten en waterkwaliteit, Natuurhistorische Bibliotheek no 45,
Stichting Uitgeverij Koninklijke Nederlandse Natuurhistorische Vereniging (1988).
[2] M.J.R. Cals, J.G.M. Roelofs. Effecten van gebiedsvreemd water in het Noorderpark. Landinrichting 29, 21–26
(1989).
[3] J.G.M. Roelofs, M.J.R. Cals. Effecten van inlaat van gebiedsvreemd water op de waterkwaliteit en vege-
tatieontwikkeling in laag- en hoogveenplassen. In Proceedings Symposium Gebiedsvreemd water: Omvang en
effecten op ecosystemen, J.G.M. Roelofs (Ed.), pp. 72–86, Department of Aquatic Ecology and Biogeology,
University of Nijmegen, The Netherlands (1989).
[4] M.J.R. Cals, J.G.M. Roelofs. Mechanismen van interne eutrofiëring en alkalinisering. Utrecht Plant Ecol.
News Rep.,10, 39–46 (1990).
[5] J.G.M. Roelofs. Inlet of alkaline river water into peaty lowlands: effects on water quality and Stratiotes aloides
L. stands. Aquat. Bot.,39, 267–293 (1991).
[6] J.G.M. Roelofs, A.J.P. Smolders. Grote veranderingen in laagveenplassen door de inlaat van Rijnwater.
De Levende Natuur,94, 78–82 (1993).
[7] A.J.P. Smolders, J.G.M. Roelofs. Sulphate mediated iron limitation and eutrophication in aquatic systems.
Aquat. Bot.,46, 247–253 (1993).
[8] L.P.M. Lamers, A.J.P. Smolders, E. Brouwer, J.G.M. Roelofs. Sulfaatverrijkt water als inlaatwater? – De rol
van waterkwaliteit bij maatregelen tegen verdroging. Landschap,13, 169–180 (abstract in English) (1996).
[9] J.I. Drever. The Geochemistry of Natural Waters, Surface and Ground Water Environments, 3rd ed., Prentice
Hall, Upper Saddle River, NJ (1997).
[10] R.G. Wetzel. Limnology, W.B. Saunders, Philadelphia, PA (2001).
[11] J.M. Tiedje. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In Biology of
Anaerobic Microorganisms, A.J.B. Zehnder (Ed.), pp. 179–244, Wiley, New York (1988).
[12] M. Holmer, P. Storkholm. Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwat. Biol.,
46, 431–451 (2001).
[13] N.F. Caraco, J.J. Cole, G.E. Likens. Evidence for sulphate-controlled phosphorus release from sediments of
aquatic systems. Nature,341, 156–158 (1989).
[14] L.P.M. Lamers, H.B.M Tomassen, J.G.M.Roelofs. Sulfate-induced eutrophication and phytotoxicity in
freshwater wetlands. Environ. Sci. Technol.,32, 199–205 (1998).
[15] L.P.M. Lamers, G.E. Ten Dolle, S.T.G. Van Den Berg, S.P.J. Van Delft, J.G.M. Roelofs. Differential responses
of freshwater wetland soils to sulphate pollution. Biogeochemistry,55, 87–102 (2001).
[16] T.S. Traaen.Effects of acidity on decomposition of organic matter in aquatic environments. In Ecological impact
of acid precipitation, D. Drablos, A. Tollan (Eds), pp. 340–341, Proceedings of an International Symposium,
March, 1980, Sandeflord, Norway (1980).
[17] V.L McKinley, J.R. Vestal. Effects of acid on plant litter decomposition in an arctic lake. Appl. Environ.
Microbiol.,43, 1199–1195 (1982).
[18] T.C.M. Brock, J.J. Boon, B.G.P. Paffen. The effects of the season and of water chemistry on the decomposition
of Nymphaea alba L.; weight loss and pyrolysis mass spectrometry of the particulate matter. Aquat. Bot.,22,
197–229 (1985).
[19] C.J. Kok, H.W.G. Meesters, A.J. Kempers. Decomposition rate, chemical composition and nutrient recycling
of Nymphaea alba L. floating leaf blade detritus as influenced by pH, alkalinity and aluminium in laboratory
experiments. Aquat. Bot.,37, 215–227 (1990).
[20] C.J. Kok, G. Van der Velde. The influence of selected water quality parameters on the decay rate and exoenzy-
matic activity of detritus of Nymphaea alba L. floating leaf blades in laboratory experiments. Oecologia,88,
311–316 (1991).
[21] C.J. Kok, W. Haverkamp, H.A. Van der Aa. Influence of pH and the growth and leaf maceration ability of fungi
involved in the decomposition of floating leaves of Nymphaea alba L. in an acid water. J. Gen. Microbiol.,
138, 103–108 (1992).
[22] C.J. Kok, C.H.J. Hof, J.P.M. Lenssen, G.Van der Velde. The influence of pH on concentrations of protein and
phenolics and resource quality of decomposing floating leaf material of Nymphaea alba L. (Nymphaeaceae)
for the detritivore Asellus aquaticus (L.). Oecologia,91, 229–234 (1992).
[23] C.J. Kok, G. Van der Velde. Decomposition and macroinvertebrate colonization of aquatic and terrestrial leaf
material in alkaline and acid still water. Freshwat. Biol.,31, 65–75 (1994).
[24] L.P.M. Lamers, C. Farhoush, J.M.Van Groenendael, J.G.M. Roelofs. Calcareous groundwater raises bogs; the
concept of ombrotrophy revisited. J. Ecol. 87, 639–648 (1999).
[25] A.J.P. Smolders, H.B.M. Tomassen, L.P.M Lamers, B.P. Lomans, J.G.M. Roelofs. Peat bog restoration by
floating raft formation: the effects of groundwater and peat quality. J. Appl. Ecol.,39, 391–401 (2002).
[26] C.J. Kok, B.J. Van de Laar. Influence of pH and buffering capacity on the decomposition of Nymphaea alba L.
detritus in laboratory experiments: a possible explanation for the inhibition of decomposition at low alkalinity.
Verhandl. Int. Vereinig. Theor. Angew. Limnol.,24, 2689–2692 (1991).
[27] M.M. Van Katwijk, J.G.M. Roelofs. Vegetaties van waterplanten in relatie tot het milieu, Laboratorium voor
Aquatische Oecologie, Katholieke Universiteit Nijmegen, 133 pp. (1988).
[28] A.J.P. Smolders. Mechanisms involved in the decline of aquatic macrophytes in the Netherlands; in particular
of Stratiotes aloides L., PhD thesis, University of Nijmegen, Nijmegen (1995).
Internal eutrophication 109
[29] L.P.M. Lamers, A.J.P. Smolders, J.G.M. Roelofs. The restoration of fens in the Netherlands. Hydrobiologia,
478, 107–130 (2002).
[30] A.J.P. Smolders, J.G.M. Roelofs. Internal eutrophication, iron limitation and sulphide accumulation due to the
inlet of river Rhine water in peaty shallow waters in the Netherlands. Arch. Hydrobiol.,133, 349–365 (1995).
[31] G. Van der Velde, G.Van Urk, F.W.BVan den Brink, F. Colijn, W.A. Bruggeman, R.S.E.W. Leuven. Rein Rijn-
water, een sleutelfactor in chemisch oecosysteemherstel, In Flora en Fauna chemisch onder druk, G. Hekstra,
F.J.M. Van Linden (Eds), pp. 231–266, Pudoc Wageningen (1991).
[32] P.J. Stuyfzand. Hydrochemistry and hydrology of coastal dune area of the Western Netherlands. PhD thesis,
University of Amsterdam, Amsterdam (1993).
[33] E.C.H.E.T. Lucassen, A.J.P. Smolders, A.L. Van der Salm, J.G.M. Roelofs. High groundwater nitrate
concentrations inhibit eutrophication of sulphate-rich freshwater wetlands. Biogeochemistry,67, 249–267
(2004).
[34] T.M. Iversen, K. Grant, K. Nielsen. Nitrogen enrichment of European inland and marine waters with special
attention to Danish policy measures. Environ. Pollut.,102, 771–780 (1998).
[35] N. Van Breemen, P.A. Burrough, E.J.Velthorst, H.F. Van Dobben, T. De Wit, T.B. Ridder,H.F.R. Reijnders. Soil
acidification from atmospheric ammonium sulphate in forest canopy throughfall. Nature 299, 548–550 (1982).
[36] J.G.M. Roelofs, A.J. Kempers, A.L.F.M. Houdijk, J. Jansen. The effect of air-borne ammonium sulphate on
Pinus nigra var. maritima in the Netherlands. Plant Soil 84, 45–56 (1985).
[37] F. Hagedorn, P. Schleppi, J. Bucher, H. Flühler. Retention and leaching of elevated N deposition in a forest
ecosystem with gleysols. Water Air Soil Pollut.,129, 119–142 (2001).
[38] W. Kölle, O. Strebel, J. Böttcher. Formation of sulfate by microbial denitrification in a reducing aquifer. Water
Supply,3, 33–40 (1985).
[39] R. Aravena, W.D.Robertson. Use of multiple tracers to evaluate denitrification in ground water: Study of nitrate
from a large-flux septic system plume. Ground Water,36, 975–982 (1998).
[40] H. Pauwels, W. Klopmann, J.C. Foucher, A. Martelat, V. Fritsche. Field tracer test for denitrification in a
pyrite-bearing aquifer. Appl. Biogeochem.,13, 767–787 (1998).
[41] A.J. Tesoriero, H. Liebscher, S.E. Cox. Mechanisms and rates of denitrification in an agricultural watershed:
Electron and mass balance along ground water flow paths. Water Res.,36, 1545–1559 (2000).
[42] J.M. Van Steenwijk. De chemie van het grondwater in het eerste watervoerend pakket rond het pompstation
Vierlingsbeek, KIWA, SWE 86.018, The Netherlands (1986).
[43] B. Beltman, T.G. Rouwenhorst, M.B. Van Kerkhoven, T. Van der Krift, J.T.A. Verhoeven. Internal eutroph-
ication in peat soils through competition between chloride and sulphate with phosphate for binding sites.
Biogeochemistry,50, 183–194 (2000).
[44] J.I. Sperber. Release of phosphate from soil minerals by hydrogen sulphide. Nature,181, 934 (1958).
[45] A.J.P. Smolders, J.G.M. Roelofs. The roles of internal iron hydroxide precipitation, sulphide toxicity and oxi-
dizing ability in the survival of Stratiotes aloides roots at different iron concentrations in sediment pore water.
New Phytol.,133, 253–260 (1996).
[46] E.E. Roden, J.W. Edmonds. Phosphate mobilization in iron-rich anaerobic sediments: microbial Fe(III) oxide
reduction versus iron-sulfide formation. Arch. Hydrobiol.,139, 347–378 (1997).
[47] A.J.P. Smolders, L.P.M. Lamers, M. Moonen, K. Zwaga, J.G.M. Roelofs. Controlling the phosphate release
from phosphate-enriched sediments by adding various iron compounds. Biogeochemistry,54, 219–228 (2001).
[48] L.P.M. Lamers, S-J. Falla, E.M. Samborska, I.A.R. Van Dulken, G. Van Hengstum, J.G.M. Roelofs. Factors
controlling the extent of eutrophication and toxicity in sulfate-polluted freshwater wetlands. Limnol. Oceanogr.,
47, 585–593 (2002).
[49] A.J.P. Smolders, R.C. Nijboer, J.G.M. Roelofs. Prevention of sulphide accumulation and phosphate mobiliza-
tion by the addition of iron(II) chloride to a reduced sediment: an enclosure experiment. Freshwat. Biol.,34,
559–568 (1995).
[50] A.J.P. Smolders, J.G.M. Roelofs, G. Van der Velde. Iron deficiency in Nymphoides peltata owing to the
exhaustion of dissolved iron in anaerobic sediments. Aquat. Bot.,47, 349–353 (1994).
[51] E.B. Adema, H. Grootjans. Positive-feedback mechanisms: plant change abiotic soil parameters in wet
calcareous dune slacks. Plant Ecol.,167, 141–149 (2003).
[52] C.H. Mortimer. The exchange of dissolved substances between mud and water in lakes. I and II. J. Ecol.,29,
280–329 (1941).
[53] C.H. Mortimer. The exchange of dissolved substances between mud and water in lakes III and IV. J. Ecol.,30,
147–201 (1942).
[54] R.D. Gulati, E. Van Donk. Lakes in the Netherlands, their origin, eutrophication and restoration: state-of-the-art
review. Hydrobiologia 478, 73–106 (2002).
[55] M. Scheffer, R. Portielje, L. Zambrano. Fish facilitate wave resuspension of sediment. Limnol. Oceanogr.,48,
1920–1926 (2003).
[56] M.J.S. Bellemakers, M. Maessen. Effects of alkalinity, acidity and external sulphate and phosphorus load on
water chemistry in the ‘Naardermeer’. Water Air Soil Pollut.,101, 3–14 (1998).
[57] E. Brouwer, J. Soontiens, R. Bobbink, J.G.M. Roelofs. Sulphate and bicarbonate as key factors in sediment
degradation and restoration of Lake Banen. Aquat. Conserv. Mar. Freshwat. Ecosyst.,9, 121–132 (1999).
[58] E.C.H.E.T. Lucassen,A.J.P. Smolders, J.Van de Crommenacker,J.G.M. Roelofs. Effects of stagnating sulphate-
rich groundwater on the mobility of phosphate in freshwater wetlands: a field experiment. Arch. Hydrobiol.,
160, 117–131 (2004).
110 A. J. P. Smolders et al.
[59] L.P.M. Lamers, S.M.E. Van Roozendaal, J.G.M. Roelofs. Acidification of freshwater wetlands: combined
effects of non-airborne sulfur pollution and desiccation. Water Air Soil Pollut.,105, 95–106 (1998).
[60] A.J.P. Smolders, J.G.M. Roelofs, C. Den Hartog. Possible causes for the decline of the water soldier (Stratiotes
aloides L.) in the Netherlands. Arch. Hydrobiol.,136, 327–342 (1996).
[61] A.J.P. Smolders, L.P.M. Lamers, C. Den Hartog, J.G.M. Roelofs. Mechanisms involved in the decline of
Stratiotes aloides L. in the Netherlands: sulphate as a key variable. Hydrobiologia,506/509, 603–610 (2003).
[62] M.J.H. De Lyon, J.G.M. Roelofs. Waterplanten in relatie tot waterkwaliteit en bodemgesteldheid. Deel 1 and 2.
Laboratorium voor Aquatische Oecologie, Katholieke Universiteit Nijmegen, Nijmegen (1986).
[63] F. Scheffer, P. Schachtschabel. Lehrbuch der Bodenkunde, Enke, Stuttgart (1992).
[64] K.S. Straub, M. Benz, B. Schink, F. Widdel.Anaerobic, nitrate dependent microbial oxidation of ferrous iron.
Appl. Environ. Microbiol.,62, 1458–1460 (1996).
[65] J.L. Nielsen, P.H. Nielsen. Microbial nitrate-dependent oxidation of ferrous iron in activated sludge. Environ.
Sci. Technol.,32, 3556–3561 (1998).
[66] K.A. Weber, F.W. Picardal, E.E. Roden. Microbially catalyzed nitrate-dependent oxidation of biogenic
solid-phase Fe(II) compounds. Environ. Sci. Technol.,35, 1644–1650 (2001).
[67] D. Uhlmann, L. Paul. Causes and effects of ‘nitrate saturation’ in phosphate-deficient water bodies. Water Sci.
Technol.,30, 281–288 (1994).
[68] A.J.P. Smolders, R.J.J. Hendriks, H.M. Campschreur, J.G.M. Roelofs. Nitrate induced iron deficiency chlorosis
in Juncus acutiflorus. Plant Soil,196, 37–45 (1997).
[69] H. Klapper. Restaurierung von Seen. In Ingenieurökologie 2.Aufl., K.F. Busch, D. Uhlmann, G. Weise (Eds),
pp. 278–284, Fischer, Jena (1989).
[70] W. Ripl. Biochemical oxidation of polluted lake sediment with nitrate. Ambio,5, 132–135 (1976).
[71] H.L. Golterman. The influence of FeS on the denitrification rate. Verhandl. Int. Vereinig. Theor. Angew. Limnol.,
24, 3025–3028 (1991).
[72] H.L. Golterman. The labyrinth of nutrient cycles and buffers in wetlands: results based on research in the
Camargue (southern France). Hydrobiologia,315, 39–58 (1995).
[73] E.C.H.E.T. Lucassen. Biogeochemical constraints for restoration of sulphate-rich fens. PhD thesis University
of Nijmegen, Nijmegen (2004).
[74] A.W. Boxman, A.H.F. Stortelder. Hoe natter, hoe beter? De invloed van het waterpeil bij maatregelen tegen
verdroging in elzenbroekbossen. Vakblad Natuurb.,5, 75–77 (2000).
[75] A.J.M. Smits, P. Laan, R.H. Thier, G. Van der Velde. Root aerenchyma, oxygen leakage patterns and alcoholic
fermentation ability of the roots of some nymphaeid and isoetid macrophytes in relation to the sediment type
of their habitat. Aquat. Bot.,38, 3–17 (1990).
[76] A.J.P. Smolders, E.C.H.E.T. Lucassen, J.G.M. Roelofs. The isoetid environment: biogeochemistry and threats.
Aquat. Bot. 73, 325–350 (2002).
[77] E.B. Adema, H. Van Gemerden, A.P. Grootjans. Is succession in wet calcareous dune slacks affected by free
sulphide? J. Veget. Sci.,14, 153–162 (2003).
[78] W.H. Patrick, R.A. Khalid. Phosphate release and sorption by soils and sediments: effect of aerobic and
anaerobic conditions. Science,186, 53–55 (1974).
[79] N. Risgaard-Petersen, K. Jensen. Nitrification and denitrification in the rhizosphere of the aquatic macrophyte
Lobelia dortmanna L. Limnol. Oceanogr.,42, 529–537 (1997).
[80] C.J. Richardson. Mechanisms controlling phosphorus retention capacity in freshwater wetlands. Science,228,
1424–1427 (1985).
[81] H.L. Golterman. The calcium- and iron bound phosphate phase diagram. Hydrobiologia,159, 149–151 (1988).
[82] E.C.H.E.T. Lucassen, A.J.P. Smolders, J.G.M. Roelofs. Potential sensitivity of mires to drought, acidification
and mobilisation of heavy metals: the sediment S/(Ca +Mg) ratio as diagnostic tool. Environ. Pollut.,120,
635–646 (2002).
[83] W. Stumm, J.J. Morgan. Aquatic Chemistry, an Introduction Emphasizing Chemical Equilibria in Natural
Waters, 2nd ed., Wiley, New York (1981).
[84] E.C.H.E.T. Lucassen, A.J.P. Smolders, J.G.M. Roelofs. Effects of temporary desiccation on the mobility of
phosphorus and metals in sulphur-rich fens: differential responses of sediments and consequences for water
table management. Wetland Ecol. Manage.,13, 135–148 (2005).
[85] E.C.H.E.T. Lucassen, A.J.P. Smolders, L.P.M. Lamers, J.G.M. Roelofs. Water table fluctuations and ground-
water supply are important in preventing phosphate eutrophication in sulphate-rich fens: Consequences for
wetland restoration. Plant Soil,269, 109–115 (2005).
[86] K.L. Burley, E.E. Prepas, P.A. Chambers. Phosphorus release from sediments in hardwater eutrophic lakes:
the effects of redox-sensitive and -insensitive chemical treatments. Freshwat. Biol.,46, 1061–1064 (2001).
[87] J. Shapiro, V. Lamarra, M. Lynch. Biomanipulation: an ecosystem approach to lake restoration. In Water Qual-
ity Management through Biological Control, P.L. Brezonik, J.L. Fox (Eds), pp. 85–96, University of Florida,
Gainesville, FL (1975).
[88] E. Jeppesen, J.P. Jensen, P. Kristensen, M. Søndergaard, E. Mortensen, O. Sortkjaer, O.K. Olrik. Fish mani-
pulation as a lake restoration tool in shallow, eutrophic, temperate lakes 2: threshold levels, long-term stability
and conclusions. Hydrobiologia,200/201, 219–227 (1990).
[89] M. Scheffer, S.H. Hosper, M.-L. Meijer, B. Moss, E. Jeppesen.Alternative equilibria in shallow lakes. TREE,
8, 275–278 (1993).
Internal eutrophication 111
[90] S.H. Hosper. Clearing lakes –An ecosystem approach to the restoration and management of shallow lakes in
the Netherlands. PhD thesis Wageningen Agricultural University, Wageningen (1997).
[91] E. Van Donk, W. Van de Bund. Impact of submerged macrophytes including charophytes on phyto- and
zooplankton communities: allelopathy versus other mechanisms. Aquat. Bot.,72, 261–274 (2002).
[92] R.D. Gulati, E.H.R.R. Lammens, M.-L. Meijer, E. Van Donk. Biomanipulation Tool for Water Management,
Developments in Hydrobiology 61, Kluwer Academic, Dordrecht (1990).
[93] B. Moss. Ecology of Fresh Waters –Man and Medium, 3rd edition, Blackwell Scientific, Oxford (1998).
[94] M.-L. Meijer, I. De Boois, M. Scheffer, R. Portielje, H. Hosper. Biomanipulation in shallow lakes in the
Netherlands: an evaluation of 18 case studies. Hydrobiologia,408/409, 13–30 (1999).
[95] M. Klinge, M.P. Grimm, S.H. Hosper. Eutrophication and ecological rehabilitation of Dutch lakes: presentation
of a new conceptual framework. Water Sci. Technol.,31, 207–218 (1995).
[96] M.-L. Meijer. Biomanipulation in the Netherlands – 15 Years of Experience. PhD thesis, Wageningen
Agricultural University, Wageningen (2000).
[97] E.E. Prepas, J. Babin, T.P. Murphy, P.A. Chambers, G.J. Sandland, A. Ghadouani, M. Serediak. Long-term
effects of successive Ca(OH)3and CaCO3treatments on the water quality of two eutrophic hardwater lakes.
Freshwat. Biol.,46, 1089–1103 (2001).
[98] E.E. Prepas, B. Pinel-Alloul, P.A. Chambers,T.P. Murphy, S. Reedyk, G. Sandland, M. Serediak. Lime treatment
and its effects on the chemistry and biota of hardwater eutrophic lakes. Freshwat. Biol.,46, 1059–1060 (2001).
[99] G.D. Cooke, R.T. Health, R.H. Kennedy, M.R. McComas. Change in lake trophic state and internal phosphorus
release after aluminium sulfate application. Water Res. Bull.,18, 699–705 (1982).
[100] P.C.M. Boers. The release of dissolved phosphorus from lake sediments. PhD thesis,Wageningen Agricultural
University, Wageningen (1991).
[101] G.D. Cooke, E.B. Welch, A.B. Martin, D.G. Fulmer, G.C. Schrieve. Effectiviness of Al, Ca and Fe salts for
control of internal phophorus loading in shallow and deep lakes. Hydrobiologia,25, 323–335 (1993).
[102] E.B. Welch, G.D. Cooke. Effectiveness and longevity of phosphorus inactivation with Alum. Lake Reserv.
Manage.,15, 5–27 (1999).
[103] E. Rydin, E.B. Welch. Aluminum dose required to inactivate phosphate in lake sediments. Water Res.,32,
2969–2976 (1998).
[104] W.T. Dickson. Some effects of the acidification of Swedish lakes. Verhandl. Int. Vereinig. Theor. Angew. Limnol.,
20, 851–856 (1978).
[105] B.O. Rosseland, I.A. Blakar, A. Bulger, F. Kroglund, A. Kvellstad, E. Lydersen, D.H. Houghton, B. Salbu,
M. Staurnes, R. Vogt. The mixing zone between limed and acidic river waters: complex aluminium chemistry
and extreme toxicity for salmonids. Environ. Pollut.,78, 3–8 (1992).
[106] E. Brouwer, J.G.M. Roelofs. Oligotrophication of acidified, nitrogen-saturated softwater lakes after dredging
and controlled supply of alkaline water. Arch. Hydrobiol.,155, 83–97 (2002).
[107] G. Boedeltje, A.J.P. Smolders, L.P.M. Lamers, J.G.M. Roelofs. Interactions between sediment propagule banks
and sediment nutrient fluxes explain floating plant dominance in stagnant shallow water. Arch. Hydrobiol.,162,
349–362 (2005).
[108] H.L. Golterman. Fractionation of sediment phosphate with chelating compounds: a simplification, and
comparison with other methods. Hydrobiologia,335, 87–98 (1996).
