ArticlePDF Available

Abstract and Figures

Lakes can be sources or sinks of carbon, depending on local conditions. Recent studies have shown that the CO 2 efflux increases when lakes recover from eutrophication, mainly as a result of a reduction in phytoplankton biomass, leading to less uptake of CO 2 by producers. We hypothesised that lake restoration by removal of coarse fish (biomanipulation) or invasion of mussels would have a similar effect. We studied 14–22 year time series of five temperate Danish lakes and found profound effects on the calculated CO 2 efflux of major shifts in ecosystem structure. In two lakes, where limited colonisation of submerged macrophytes occurred after biomanipulation or invasion of zebra mussels (Dreissena polymorpha), the efflux increased significantly with decreasing phytoplankton chlorophyll a. In three lakes with major interannual variation in macrophyte abundance, the efflux declined with increasing macrophyte abundance in two of the lakes, while no relation to macrophytes or chlorophyll a was found in the third lake, likely due to high groundwater input to this lake. We conclude that clearing water through invasive mussels or lake restoration by bioma-nipulation may increase the CO 2 efflux from lakes. However, if submerged macrophytes establish and form dense beds, the CO 2 efflux may decline again.
This content is subject to copyright. Terms and conditions apply.
SHALLOW LAKES
Major changes in CO
2
efflux when shallow lakes shift
from a turbid to a clear water state
Erik Jeppesen .Dennis Trolle .Thomas A. Davidson .Rikke Bjerring .
Martin Søndergaard .Liselotte S. Johansson .Torben L. Lauridsen .
Anders Nielsen .Søren E. Larsen .Mariana Meerhoff
Received: 14 April 2015 / Revised: 26 August 2015 / Accepted: 29 August 2015 / Published online: 23 October 2015
ÓSpringer International Publishing Switzerland 2015
Abstract Lakes can be sources or sinks of carbon,
depending on local conditions. Recent studies have
shown that the CO
2
efflux increases when lakes recover
from eutrophication, mainly as a result of a reduction in
phytoplankton biomass,leading to less uptake of CO
2
by
producers. We hypothesised that lake restoration by
removal of coarse fish (biomanipulation) or invasion of
mussels would have a similar effect. We studied
14–22 year time series of five temperate Danish lakes
and found profound effects on the calculated CO
2
efflux
of major shifts in ecosystem structure. In two lakes,
where limited colonisation of submerged macrophytes
occurred after biomanipulation or invasion of zebra
mussels (Dreissena polymorpha), the efflux increased
significantly with decreasing phytoplankton chlorophyll
a. In three lakes with major interannual variation in
macrophyte abundance, the efflux declined with
increasing macrophyte abundance in two of the lakes,
while no relation to macrophytes or chlorophyll awas
found in the third lake, likely due to high groundwater
input to this lake. We conclude that clearing water
through invasive mussels or lake restoration by bioma-
nipulation may increase the CO
2
efflux from lakes.
However, if submerged macrophytes establish and form
dense beds, the CO
2
efflux may decline again.
Keywords Air–water CO
2
flux Recovery
Eutrophication Macrophytes Zebra mussel Lake
metabolism
Guest editors: M. Bekliog
˘lu, M. Meerhoff, T. A. Davidson,
K. A. Ger, K. E. Havens & B. Moss / Shallow Lakes in a Fast
Changing World
Electronic supplementary material The online version of
this article (doi:10.1007/s10750-015-2469-9) contains supple-
mentary material, which is available to authorized users.
E. Jeppesen (&)D. Trolle T. A. Davidson
R. Bjerring M. Søndergaard L. S. Johansson
T. L. Lauridsen A. Nielsen M. Meerhoff
Lake Ecology Section, Department of Bioscience and the
Arctic Research Centre, Aarhus University, Aarhus,
Denmark
e-mail: ej@dmu.dk; ej@bios.au.dk
E. Jeppesen D. Trolle T. L. Lauridsen S. E. Larsen
Sino-Danish Centre for Education and Research (SDC),
Beijing, China
S. E. Larsen
Catchment Science and Environmental Management
Section, Department of Bioscience, Aarhus University,
Aarhus, Denmark
S. E. Larsen M. Meerhoff
Departamento de Ecologı
´a Teo
´rica y Aplicada, Centro
Universitario de la Regio
´n Este-Facultad de Ciencias,
Universidad de la Repu
´blica, Maldonado, Uruguay
123
Hydrobiologia (2016) 778:33–44
DOI 10.1007/s10750-015-2469-9
Introduction
Lakes can act as either sources or sinks of carbon
depending, among several processes, on the balance
between photosynthesis and ecosystem respiration as
well as the external nutrient input (Cole et al., 1994,
2000). The importance of lakes in the global carbon
cycle is not yet fully resolved (Moss et al., 2011;
Raymond et al., 2013) because most models have
typically focused on marine, terrestrial and atmo-
spheric compartments. However, our understanding of
the role of freshwaters as a source or sink of CO
2
is
increasing (Dean & Gorham, 1998; Stallard, 1998;
Cole et al., 2007, Cole, 2013; Barros et al., 2011).
It is now evident that inland waters, and lakes in
particular, can play an important role in CO
2
exchange
with the atmosphere (Tranvik et al., 2009). Lakes are
often supersaturated with CO
2
(e.g. Kling et al., 1992;
Cole et al., 1994; Kosten et al., 2010), thereby acting as
aCO
2
source to the atmosphere. The saturation level is
greatly influenced by primary production, which
depletes CO
2
through photosynthesis and increases
pH (Talling, 1976). With increasing eutrophication,
phytoplankton productivity increases and water CO
2
decreases (Wetzel, 2001). Furthermore, more carbon
is buried in the lake sediments in eutrophic lakes
(Anderson et al., 2014) and the CO
2
efflux is therefore
reduced. Conversely, the efflux is expected to increase
again as lakes recover from eutrophication (Provoost
et al., 2010) after reductions in the external nutrient
input. For instance, substantial reductions in the
nutrient loading to four Danish lakes resulted in an
increase in annual average CO
2
effluxes of[30% over
a 20-year period, concurrently with decreasing phyto-
plankton biomass (Trolle et al., 2012). Moreover, the
largest changes in the CO
2
efflux were observed in
winter when the reduction in chlorophyll a(Chl a) was
most pronounced, while the summer efflux was lower
and at times negative as internal phosphorus loading
kept phytoplankton biomass relatively high during the
warmer months (Trolle et al., 2012).
Shifts in trophic structure may ultimately affect the
composition and nature of primary producers and
consequently net productivity, water pH and CO
2
efflux.
In an attempt to obtain clear water conditions following
nutrient loading reduction, plankti-benthivorous fish may
be removed (biomanipulation) to enhance zooplankton
grazing on phytoplankton and to reduce physical
disturbance of the sediments (Carpenter et al., 1998;
Jeppesen et al., 2012), thereby speeding up recovery. A
reduction in phytoplankton Chl awould be expected to
result in higher CO
2
efflux, but, at least in the short term,
one might also expect that a reduction in disturbance of
the sediment would reduce decomposition and enhance
net accumulation in the sediment, potentially counter-
acting the increased CO
2
efflux.
Phytoplankton biomass and production may also be
notably affected by other changes in the trophic web,
such as the introduction of invasive key-stone species.
Over the last few decades, many lakes worldwide
have been colonised by invasive bivalves, including
golden mussel (Limnoperna fortune (Dunker, 1857))
and zebra mussel (Dreissena polymorpha (Pallas,
1771)) (e.g. Strayer et al., 1999; Karatayev et al.,
2007). The establishment of zebra mussels, in partic-
ular, is often followed by major changes, particularly
reduced phytoplankton biomass and increased water
clarity (Idrisi et al., 2001; Mayer et al., 2002; Higgins
& Vander Zanden, 2010). As with biomanipulation,
such changes can lead to higher CO
2
efflux although
faeces from the mussels might enhance net carbon
accumulation (Stewart et al., 1998).
In turn, improving water clarity in shallow lakes
provides an opportunity for submerged macrophytes
to increase in abundance or (re)colonise (Moss, 1990;
Moss et al., 1996; Scheffer et al., 1993). In dense
macrophyte stands, water circulation can be low and
the concentration of CO
2
may drop to very low levels
during daytime, most markedly in the upper part of the
macrophyte stand (Jones et al., 1996). Many sub-
merged macrophytes can use bicarbonate (HCO
3), but
CO
2
is generally the preferred carbon source (Jones,
2005). CO
2
uptake by the macrophytes and associated
periphyton can also lead to precipitation of calcium
carbonate (CaCO
3
). Moreover, lakes with abundant
macrophytes may store additional carbon due to
accumulation of plant material in the sediments
(Carpenter, 1981). Therefore, presence of submerged
plants may increase the likelihood of a lake being a
carbon sink. We therefore hypothesised that although
the CO
2
efflux should increase in eutrophic lakes in the
early phase after nutrient loading reduction, owing to
reduction in phytoplankton biomass, this process
should be reversed if submerged macrophytes become
abundant and permanently established. Very high
cover and biomasses of submerged macrophytes under
34 Hydrobiologia (2016) 778:33–44
123
mesotrophic to eutrophic conditions are only possible
in shallow lakes (Wetzel, 2001) where the water depth
is potentially low enough to allow light penetration to
the bottom over large areas. Thus, it may be hypoth-
esised that the positive effect on carbon sequestration
of macrophyte establishment following improvements
in water clarity is mainly of importance in shallow
lakes.
To investigate the effect of substantial changes in
trophic structure on the CO
2
efflux from temperate
shallow lakes, we estimated the CO
2
efflux using data
from long-term studies of five Danish lakes before and
after major shifts in trophic structure (fish removal,
macrophyte biomass changes and zebra mussel
colonisation).
Methods
Study sites
All five study lakes are eutrophic, shallow and
polymictic. Basic data are given in Table 1. Lake
Faarup was colonised by zebra mussels in the 1990s,
mussel larvae being observed for the first time in 1993,
and veliger larvae have been present in the plankton
from 1998 onwards (Jeppesen et al., 2012). In 2000,
their density was up to 1,300 ind. m
-2
. Since 1995, a
major decrease has occurred in summer mean Chl a,
TP, TN, and annual mean Chl a, but not in annual
mean TP and TN (Jeppesen et al., 2012). Accordingly,
water transparency measured as Secchi depth has
increased, but macrophytes have very low cover. As
the external loading of TN and TP has not changed
during the study period, the drastic changes can be
attributed to the colonisation and a gradual increase in
zebra mussel densities (Jeppesen et al., 2012).
Lake Væng receives about 90% of its water from
groundwater (Kidmose et al., 2013) and the water
residence time is very short (Table 1). For many years,
the lake received waste water from a local community.
Following diversion of this loading in 1981, the lake
remained turbid (Søndergaard et al., 1990) and was
therefore biomanipulated during 1986–1988 by
removing approximately 50% (4 tonnes) of the fish
stock (almost exclusively bream, Abramis brama L.,
and roach, Rutilus rutilus L.). Subsequently, phyto-
plankton Chl aand water turbidity decreased substan-
tially and the lake was colonised by submerged
macrophytes, first Potamogeton crispus L. and then
Elodea canadensis Michx., the latter completely
covering the lake within a 1–2 year period (Lauridsen
et al., 1994). However, from 1998 onwards, macro-
phytes largely disappeared. Concurrently, the abun-
dance of roach and small perch (Perca fluviatilis L.)
increased (Jeppesen et al., 2012). In an attempt to shift
the lake back to the clear state, 2.7 tonnes (68% of the
first biomanipulation effort) of bream and roach were
removed during 2007–2009. The concentration of Chl
adecreased and the coverage of submerged macro-
phytes increased from \1% to ca. [70%, and since
2009 the biomasses of roach and bream have remained
low compared with the years prior to the fish
manipulation (Jeppesen et al., 2012).
Lake Engelsholm was also subjected to nutrient
loading reduction and showed delayed recovery
(Bjerring et al., 2013). Restoration by biomanipulation
was conducted in 1992–1994. Nineteen tonnes of
cyprinid fishes were removed and their estimated
biomass subsequently decreased from 675 to
150–300 kg ha
-1
(Jeppesen et al., 2012). Biomanip-
ulation led to a substantial reduction of phytoplankton
Chl a, total phosphorus (TP) and total nitrogen (TN),
as well as an increase in Secchi depth (Liboriussen
et al., 2007). Submerged macrophyte coverage has
Table 1 Physical data on the five study lakes including information on phenomena studied
Lake Lake
area
(km
2
)
Lake
catchment
area (km
2
)
Lake
mean
depth (m)
Lake
maximum
depth (m)
Water
residence
time (years)
Events
Faarup 0.99 13.2 5.6 11.1 0.6 Zebra mussel invasion
Væng 0.16 9 1.2 1.9 0.06 Biomanipulation
Engelsholm 0.44 15.2 2.4 6.1 0.73 Biomanipulation
Arreskov 3.17 24.8 1.9 3.6 1.1 Fish kill and biomanipulation
Stigsholm 0.21 0.8 1.2 0.015 Natural variation in plant coverage
Hydrobiologia (2016) 778:33–44 35
123
generally been very low, both before and during the
early years following biomanipulation. However,
during 2007–2010 the coverage increased gradually
from 2 to 12%.
Lake Arreskov received untreated sewage from the
1950s to the 1980s, leading to severe eutrophication.
Sewage was diverted in 1983. A major fish kill
occurred during autumn and winter 1991. Four tonnes
of cyprinids were removed in 1995, and the lake was
stocked with under-yearling piscivores (pike, Esox
lucius L.), in total 141 ind ha
-1
in 1993 and 1995.
Cyprinid biomass was calculated as 172 kg ha
-1
in
1987 and 71 kg ha
-1
in 1995 (Sandby & Hansen,
2007). In general, Lake Arreskov has shown large
inter-annual alternations in ecological state (sensu
Scheffer et al., 1993), exhibiting high water clarity and
high abundance of submerged vegetation in some
years, for instance 1996–1998 and 2003–2011, and
limited submerged vegetation and, consequently,
turbid water and dominance of cyanobacteria in other
years, for example 1995 and 1999–2002 (Nielsen
et al., 2014). The dominant submerged plant species
were Zannichellia palustris L., Potamogeton crispus
L., Potamogeton pectinatus L., Chara vulgaris L. and
Chara globularis L.. In other years, Ceratophyllum
demersum L. made a large contribution to the biomass.
Lastly, Lake Stigsholm has also fluctuated between
alternative states (i.e. a macrophyte-rich clear water
state and a macrophyte-poor turbid state, Scheffer
et al., 1993) since the 1980s, the dominant submerged
macrophyte species being P. pectinatus, P. berchtoldii
L. Callitriche sp. and Elodea canadensis L. as well as
filamentous algae (Jeppesen et al., 1992, 1998;
Søndergaard et al., 1998).
Chemical analyses
In all lakes depth-integrated samples were taken from
the photic zone, minimum 19 times annually, and
analysed according to standard methods (Kronvang
et al., 1993). Basic chemical data on the lakes are
given in Table 2.
Submerged macrophyte coverage
Depending on lake area, aquatic macrophytes were
inspected at 30–200 equidistant observation points
situated along transects covering the entire lake area.
At each observation point, percentage macrophyte
coverage and species composition were determined
using an underwater viewing box. Total macrophyte
coverage for the lake (percentage area covered, PAC)
was calculated based on the total number of equidis-
tant observations and a species list was compiled.
Observations were made once a year between 1 July
and 15 August.
Calculation of CO
2
flux across the air–water
interface
The flux of CO
2
across the air–water interface (JCO2),
which can be influx or efflux for under-saturated and
super-saturated waters, respectively, was estimated
based on the diffusion film model (Stumm & Morgan,
1996); a technique that has been documented in more
detail in Trolle et al. (2012) and also outlined in the
Supplementary Material:
JCO2ðmol cm2h1Þ¼kb
CO2ðaqÞ

KHPCO2ðairÞ

;
where kis a transport coefficient (cm h
-1
), bis a factor
expressing the chemical enhancement of diffusion,
[CO
2(aq)
] is the concentration of dissolved CO
2
(mol
l
-1
, equivalent to 10
-3
mol cm
-3
), K
H
is Henry’s law
constant (mol l
-1
atm
-1
) and PCO2ðairÞis the partial
pressure of CO
2
in the atmosphere (atm).
Following the approach of Trolle et al. (2012), the
transport coefficient (k) was estimated from relations
to wind speed (based on the average of three individual
empirical relations). The chemical enhancement of
diffusion (b), which occurs at high pH and at low wind
speeds when the stagnant boundary layer is thick, was
estimated from water temperature, pH, ionic strength
and wind speed using the approach of Bade and Cole
(2006). The actual CO
2
concentrations in water
samples were estimated from pH and alkalinity
following Kling et al. (1992) and Cole et al. (1994).
Monthly averages of atmospheric PCO2ðairÞduring
the period 1989–2010 were acquired from the Earth
System Research Laboratory (ESRL) at the Mauna
Loa Observatory, Hawaii (http://www.esrl.noaa.gov/
gmd/ccgg/trends/). Monthly averages of wind speed
during the period 1989–2010, based on a 20 920 km
data grid covering all of Denmark, were used to derive
wind speeds at the location of each individual lake.
These monthly averages were used to calculate CO
2
36 Hydrobiologia (2016) 778:33–44
123
Table 2 Average annual CO
2
efflux and environmental variables from the five lakes studied. Means of annual means are shown with SD in parenthesis
Lake Faarup Væng Engelsholm
Period Before colonisation
(1989–1992)
During early
colonisation
(1993–1995)
When
established
1996–2003)
Low
macrophyte
years
(PAC \5%)
High
macrophyte
years
(PAC [5%)
Before
biomanipulation
(1989–1991)
During
biomanipulation
(1992–1993)
After
biomanipulation
(1994–2010)
Number of years 3 3 8 9 10 3 2 17
CO
2
efflux (mg C m
-2
d
-1
) 213 (75) 247 (25) 576 (271) 716 (244) 1046 (379) 288 (219) 424 (91) 698 (295)
pH 8.37 (0.03) 8.33 (0.04) 8.15 (0.30) 7.75 (0.40) 7.89 (0.32) 8.32 (0.27) 8.29 (0.02) 8.02 (0.10)
Alkalinity (mmol l
-1
) 1.99 (0.07) 1.98 (0.07) 2.05 (0.06) 1.16 (0.07) 1.12 (0.10) 1.56 (0.15) 1.54 (0.01) 1.60 (0.08)
Chlorophyll a(ug l
-1
) 42 (7) 42 (11) 21 (10) 52 (8) 36 (25) 55 (29) 73 (6) 27 (6)
Total phosphorus (ug l
-1
) 96 (11) 90 (13) 74 (4) 96 (8) 83 (27) 98 (30) 110 (7) 53 (10)
Total nitrogen (mg l
-1
) 1.5 (0.1) 1.5 (0.1) 1.3 (0.2) 0.9 (0.2) 0.7 (0.3) 2.4 (0.7) 2.4 (0.2) 1.2 (0.2)
Submerged macrophyte
coverage, PAC (%)
\0.5 0.6 (0.3) 0.5 (0.4) 0.7(1.3) 52.5 (29.0) \1\1 1.0 (1.3)
Lake Arreskov Stigsholm
Period Before biomanipulation After biomanipuation
(PAC \5%)
After biomanipulation
(PAC [5%)
Low macrophyte years
(PAC \5%)
High macrophyte years
(PAC [5%)
Number of years 2 4 11 4 16
CO
2
efflux (mg C m
-2
d
-1
) 368 (56) 472 (124) 283 (192) 350 (155) 141 (135)
pH 8.59 (0.06) 8.32 (0.14) 8.48 (0.20) 8.28 (0.21) 8.49 (0.30)
Alkalinity (mmol l
-1
) 2.30 (0.20) 2.58 (0.09) 2.35 (0.28) 1.09 (0.09) 1.11 (0.06)
Chlorophyll a(ug l
-1
) 134 (12) 38 (19) 66 (38) 48 (10) 37 (19)
Total phosphorus (ug l
-1
) 230 (3) 111 (30) 119 (56) 98 (18) 89 (24)
Total nitrogen (mg l
-1
) 3.5 (0.6) 2.0 (0.3) 2.1 (0.6) 2.5 (0.2) 2.6 (0.3)
Submerged macrophyte coverage, PAC (%) \1 1.8 (1.8) 27.1 (19.7) 1.6 (1.1) 30.8 (23.9)
Hydrobiologia (2016) 778:33–44 37
123
fluxes on individual sampling dates, in the corre-
sponding year and month and location, after which
linear interpolation between sampling dates was used
to generate monthly averages of the CO
2
flux for the
individual lakes.
Statistical analysis
Based on monthly means, average data from May–
September (summer), October–April (winter) and
annually were analysed. We used Pearson correlation
and multiple linear regressions to analyse changes in
fluxes in relation to different environmental variables.
In order to include carry-over effects from 1 year to the
next in the regressions, the time series data were
modelled using an autoregressive process of order 1,
which means that the output of the process depends on
the previous term in the process and the error term.
The SAS procedures MODEL and AUTOREG were
applied to estimate parameters for a number of
different linear models. In the multiple regressions,
alkalinity and pH were left out as these variables were
used in the CO
2
efflux calculations.
Results
All lakes released CO
2
annually, and in the winter
season during all study years, most notably in the
largely groundwater-fed L. Væng (Fig. 1; Table 2). In
all lakes, the CO
2
efflux was significantly higher (ttest
with auto-regression included, AR(1), P\0.01) in the
colder season, from October to April, than in summer,
particularly at high pH (Fig. 1). On average, the CO
2
efflux per day was from 2.9 (L. Arreskov) to 4.4 (L.
Væng) times higher in the colder season than in
summer, and in most years in L. Stigsholm a shift
occurred from efflux in the cold season to influx of
CO
2
in summer (Fig. 1).
Multiple regressions (with auto-regression, AR(1)
included) relating the CO
2
efflux to the abundance of
the two types of primary producers: phytoplankton
biomass (expressed as Chl a) and summer macrophyte
coverage, as well as water temperature, were con-
ducted separately at summer, cold season and annual
scales (Table 3). CO
2
efflux was significantly nega-
tively related to Chl aat both summer and annual
scales in the two lakes where macrophytes did not
make a significant contribution to primary producer
biomass (i.e. L. Faarup subjected to zebra mussel
invasion and biomanipulated L. Engelsholm). When
macrophyte coverage was extensive, albeit variable,
there was a significant negative relationship between
cover and the CO
2
efflux (i.e. L. Stigsholm and L.
Arreskov). In contrast, no effect of macrophytes and a
marginal effect of phytoplankton Chl awere found in
biomanipulated L. Væng. For L. Arreskov, Chl aalso
contributed negatively to the summer CO
2
efflux.
Temperature was not retained in any of the models.
Outside the growing season (October to April) the
pattern was less clear, Chl abeing significant for L.
Faarup and PAC (summer values) for L. Væng and L.
Arreskov, respectively (Table 3).
Discussion
Reduction in fish abundance or zebra mussel coloni-
sation and associated increases in macrophyte abun-
dance had pronounced effects on the CO
2
efflux in the
lakes studied. In the two lakes without macrophyte
colonisation (L. Engelsholm, L. Faarup), we recorded
a major increase in the efflux of CO
2
associated with
the reduction in phytoplankton biomass (Chl a) and
thus in pH (Tables 2,3). High carbon release associ-
ated with either fish removal or zebra mussel coloni-
sation was maintained in years with low Chl a(Fig. 1),
indicating that a higher efflux was not simply a
temporary effect related to a sudden shift in ecosystem
structure.
A different picture was found for lakes where
macrophytes were or became abundant. In L.
Stigsholm, exhibiting large inter-annual variations in
macrophyte abundance, the CO
2
efflux was negatively
related to the coverage of submerged macrophytes
both in summer and annually. In L. Arreskov, the
release was also lower in years with high macrophyte
coverage. These are conservative estimates as the
macrophytes reduce turbulence, likely leading to
progressive overestimation of the flux with increasing
macrophyte coverage; thus, the actual effect of the
plants might be stronger. High macrophyte and
periphyton production may lead to CO
2
depletion in
the water (Jones et al., 2000). Such a CO
2
depletion
and the plant-induced reduced turbulence could result
in CO
2
influx to the lake. Supporting this view, Boll
et al. (2012) found marked inter-annual variation in
the d
13
C (indicative of the sources of carbon to the
38 Hydrobiologia (2016) 778:33–44
123
ecosystem) of zooplankton and benthic macroinver-
tebrates in L. Væng. d
13
C was higher in years with
high abundance of macrophytes than when phyto-
plankton dominated the systems. They argued that this
reflected higher CO
2
consumption by plants and
associated periphyton in macrophyte-dominated
years, resulting in low CO
2
concentrations in the
water, which in turn would lead to less discrimination
against
13
C in photosynthesis (Peterson & Fry, 1987)
and, accordingly, to a higher d
13
C content of all
primary producers, including phytoplankton and then
consumers. However, use of bicarbonate (more
enriched in
13
C than atmospheric CO
2
) by the
macrophytes may also increase d
13
C. Others have
also observed higher d
13
C of primary producers when
macrophytes are abundant (Gao et al., 2014;de
Kluijver et al., 2015). In L. Væng the relationships
between the CO
2
efflux and Chl aand PAC were weak
despite major variations in PAC during the study
period, and only outside the growing season did the
high macrophyte coverage reduce the CO
2
efflux
(Fig. 1; Table 3). Mass mortality of macrophytes
during several winters followed by a major increase
in phytoplankton (Søndergaard et al., 1997; Lauridsen,
unpublished data) may have contributed to a negative
effect of macrophytes (measured during summer) on
the CO
2
efflux during this season. The relatively weak
response in this lake may reflect a very high input of
Fig. 1 Inter-annual variation in CO
2
efflux during summer
(May–September—dark blue dots) and outside the summer
season (October to April—light blue circles) in five lakes
subjected to: zebra mussel (D. polymorpha) invasion (L.
Faarup), restoration by biomanipulation (L. Væng, L. Engel-
sholm and L. Arreskov) and natural large variations in
macrophyte coverage (L. Stigsholm). Also shown are various
environmental variables (pH, chlorophyll a) and submerged
macrophyte coverage in late summer (July–Sept) as % of lake
area. The vertical grey areas show the timing of the major
changes leading to a shift in the lake ecosystems (D. polymorpha
veliger larvae present in the plankton in L Faarup; fish removal
in L. Væng and L. Engelsholm; fish kills in L. Arreskov)
Hydrobiologia (2016) 778:33–44 39
123
CO
2
-containing groundwater (Kidmose et al., 2013),
enhancing the CO
2
efflux (Fig. 1; Table 1) (Jeppesen
et al., 2012).
The effect of increasing water clarity, through
biomanipulation or zebra mussel invasion, on the
CO
2
balance was evident, but may differ between
shallow and deep lakes (Fig. 2). In shallow lakes, a
shift from a turbid to a clear water state may enhance
macrophyte and associated periphyton growth (Sch-
effer et al., 1993), as well as the growth of other
benthic algae that take advantage of the improved
light climate (Sand-Jensen & Søndergaard, 1981).
This may largely compensate for a reduced phyto-
plankton production (Liboriussen & Jeppesen, 2003;
Vadeboncoeur et al., 2003) and thereby maintain low
levels of CO
2
in the water. For example, Liboriussen
et al. (2011) and Jeppesen et al. (unpublished data)
found only minor variation in ecosystem production
and respiration for a number of 1-m deep ponds with
dominance either by macrophytes or phytoplankton
and benthic algae. Similar evidence was derived from
high-frequency oxygen measurements in L. Væng
conducted before, during and after the second
biomanipulation (Jeppesen et al., 2012). Net produc-
tion (March 1–Nov 15) ranged between 0.49 and
0.52 mg O
2
l
-1
day
-1
in 2007–2008 before restora-
tion and became negative in 2009 (-0.65 mg O
2
l
-1
day
-1
) when the lake was in a clear state without
macrophytes, but increased to 0.23 mg O
2
l
-1
day
-1
in 2010, coinciding with extensive growth of the
submerged macrophyte E. canadensis. In contrast,
comparison of two German lakes showed higher
gross system production in a macrophyte- compared
with a phytoplankton-dominated state (Brothers
et al., 2013).
In deep lakes, however, macrophyte and benthic
algal production may be limited to near-shore areas,
and total primary production typically decreases when
the phytoplankton production in the water declines, for
instance after restoration (Vadeboncoeur et al., 2008;
Genkai-Kato et al., 2012). Accordingly, the effect of
restoration by biomanipulation will lead to different
CO
2
emissions depending on lake depth, promoting
larger CO
2
efflux in deep lakes than in shallow systems
as the pelagic primary production will not be compen-
sated for by macrophytes or benthic production.
Table 3 Multiple regression (log-transformed data) with
AR(1) auto-regression included, relating CO
2
efflux (actual
value ?300 to account for negative values) to chlorophyll
aand macrophyte coverage (in % of lake area—PAC—one
added to account for zeroes) for annual data, summer (May 1–
Oct 1) and outside the growing season (Oct 1–Apr 1). Numbers
in parentheses are SD, N is number of years included, Pis the
significance level and R
2
the explained variance
Lake Intercept Chlorophyll aMacrophyte coverage (%, PAC) NP R
2
Annual
Faarup 8.19 (0.36) -0.51 (0.12) 14 0.0008 0.65
Væng 7.92 (0.45) -0.24 (0.12) 20 0.027 0.19
Engelsholm 7.93 (0.62) -0.33 (0.17) 21 0.00006 0.43
Arreskov 6.75 (0.15) -0.16 (0.05) 14 0.0018 0.47
Stigsholm 6.48 (0.19) -0.14 (0.07) 20 0.021 0.20
May–September
Faarup 7.65 (0.45) -0.44 (0.27) 14 0.0013 0.50
Væng 5.54 (0.37) -0.23 (0.11) 19 0.006 0.06
Engelsholm 8.03 (0.48) -0.50 (0.10) 21 0.00004 0.45
Arreskov 7.59 (0.48) -0.29 (0.13) -0.21 (0.07) 14 0.0006 0.57
Stigsholm 6.21 (0.22) -0.29 (0.10) -0.39 (0.07) 20 0.00004 0.41
October–April
Faarup 8.30 (0.47) -0.52 (0.19) 14 0.0002 0.67
Væng 7.07 (0.12) -0.11 (0.04) 19 0.0011 0.74
Engelsholm 7.05 (0.14) 21 0.0062 0.08
Arreskov 6.93 (0.13) -0.14 (0.04) 14 0.0056 0.32
Stigsholm 6.39 (0.08) 23 0.96 0.88
40 Hydrobiologia (2016) 778:33–44
123
We conclude that all the lakes studied were net-
releasers of CO
2
on an annual basis despite variations
in trophic webs. Eutrophication can decrease the
relative importance of external organic matter and
promote a higher autotrophic fixation of CO
2
(carbon
sink). It may, however, also promote a higher respi-
ration (carbon source) and increased release of other
greenhouse gases with a greater warming potential
such as methane (CH
4
) (Bastviken et al., 2008) and
N
2
O (Huttunen et al., 2003) from anoxic waters and
sediments. Lake restoration by nutrient loading reduc-
tion (Trolle et al., 2012) and/or biomanipulation by
fish removal (this study) may, however, result in a
further increase in the efflux of CO
2
, at least in the
short term. So, solving one problem (eutrophication)
partly enhances, at least temporarily, another (emis-
sion of carbon, further promoting climate warming,
depending on the balance among emissions of differ-
ent greenhouse gases).
When macrophytes become abundant, as they may
in shallow lakes of intermediate and high trophic state,
a shift back to enhanced retention of CO
2
is to be
expected. Submerged macrophytes have a strong
positive impact on biodiversity (Jeppesen et al.,
2000; Declerck et al., 2005; Muylaert et al., 2010)
and at least in temperate lakes also on water clarity
(Moss, 1990; Scheffer et al., 1993). The data presented
here suggest that plants also play a key role in reducing
the CO
2
efflux from lakes, as is also evidenced in a
mesocosm study by Davidson et al. (2015).
Restoration of shallow lakes is not always accom-
panied by the establishment of submerged macro-
phytes despite sufficient water clarity (Lauridsen et al.,
2003, Jeppesen et al., 2012). Delays in (re)colonisation
have been attributed to lack of sufficient propagules
and low dispersal potential or limited connection with
other aquatic systems acting as sources (Strand &
Weisner, 2001), herbivory at an early stage of
colonisation by waterfowl (Lauridsen et al., 1993;
Søndergaard et al., 1996; Marklund et al., 2002), fish
(Prejs, 1984) or crayfish (Rodrı
´guez-Gallego et al.,
2004) and adverse impacts of herbicides from agri-
cultural catchments. Active transplantation of macro-
phytes has been recommended when macrophytes are
Fig. 2 Conceptual overview of the expected behaviour of
shallow eutrophic lakes as sources or sinks of CO
2
, from a turbid
phytoplankton-dominated state to a clear water submerged
macrophyte-dominated state through biomanipulation and
colonisation of invasive mussels (such as zebra mussels). The
width of the arrows indicates the relative strength of CO
2
efflux
and influx
Hydrobiologia (2016) 778:33–44 41
123
not easily established naturally in order to stabilise the
clear water state and enhance ecosystem quality and
biodiversity (Moss, 1990; Scheffer et al., 1993; Moss
et al., 1996; Jeppesen et al., 1998).
Based on our study, a further argument in favour of
such restoration measures is that macrophyte estab-
lishment will also reduce greenhouse gas emissions, at
least of CO
2
and perhaps also of CH
4
(Davidson et al.,
2015).
The overwhelming majority of the world’s lakes are
small and shallow (Downing et al., 2006; Verpoorter
et al., 2014) and many of them will require restoration
in the decades to come given the increasing human
demands for fresh water (Dudgeon et al., 2006;
Vo
¨ro
¨smarty et al., 2010), but restoration measures
may have profound effects on the role of lakes within
the global carbon cycle.
Acknowledgments We are grateful to CRES (Centre for
Regional Change in the Earth System), the MARS project
(Managing Aquatic ecosystems and water Resources under
multiple Stress) funded under the 7th EU Framework
Programme, Theme 6 (Environment including Climate Change),
Contract No.: 603378 (http://www.mars-project.eu), CLEAR (a
Villum Kann Rasmussen Centre of Excellence project on lake
restoration) and CIRCE (Centre of Ecoinformatics Research in
Complexityin Ecology funded by the AU IDEAS programme) for
providing financial support. MM is supported by PEDECIBA,
SNI-ANII and the L
´Ore
´al-UNESCO for Women in Science
National Award.
References
Anderson, N. J., H. Bennion & A. F. Lotter, 2014. Lake
eutrophication and its implications for organic carbon
sequestration in Europe. Global Changes in Biology 20:
2741–2751.
Bade, D. L. & J. J. Cole, 2006. Impact of chemically enhanced
diffusion on dissolved inorganic carbon stable isotopes in a
fertilized lake. Journal of Geophysical Research 111.
doi:10.1029/2004JC002684.
Barros, N., J. J. Cole, L. J. Tranvik, Y. T. Prairie, D. Bastviken,
V. L. M. Huszar, P. del Giorgio & F. Roland, 2011. Carbon
emission from hydroelectric reservoirs linked to reservoir
age and latitude. Nature Geoscience 4: 593–596.
Bastviken, D., J. J. Cole, M. L. Pace & L. Tranvik, 2008. Fates of
methane from different lake habitats: connecting whole-
lake budgets and CH
4
emissions. Journal of Geophysical
Research 113: G02024.
Bjerring, R., L.S. Johansson, M. Søndergaard, E. Jeppesen, T.L.
Lauridsen, A. Kjeldgaard, L. Sortkjær, J. Windolf & J.
Bøgestrand, 2013. Søer 2013. NOVANA. Aarhus Univer-
sitet, DCE – Nationalt Center for Miljø og Energi, 84 s. -
Videnskabelig rapport fra DCE - Nationalt Center for Miljø
og Energi nr. 76. (in Danish)
Boll, T., L. S. Johansson, T. L. Lauridsen, F. Landkildehus, M.
Søndergaard, F. Ø. Andersen & E. Jeppesen, 2012. Chan-
ges in benthic macroinvertebrate community and lake
isotope (C, N) signals following a shift from clear to turbid
water in a shallow lake. Hydrobiologia 686: 135–145.
Brothers, S. M., S. Hilt, S. Meyer & J. Ko
¨hler, 2013. Plant
community structure determines primary productivity in
shallow, eutrophic lakes. Freshwater Biology 58:
2264–2276.
Carpenter, S. R., 1981. Submersed vegetation: an internal factor
in lake ecosystem succession. The American Naturalist
118: 372–383.
Carpenter, S. R., N. F. Caraco, D. L. Correll, R. W. Howarth, A.
N. Sharpley & V. H. Smith, 1998. Nonpoint pollution of
surface waters with phosphorus and nitrogen. Ecological
Applications 8: 559–568.
Cole, J. J., 2013. Freshwater ecosystems and the carbon cycle. In
Kinne, O. (ed.), Excellence in Ecology. Book 18. Interna-
tional Ecology Institute, Oldendorf/Luhe.
Cole, J. J., N. F. Caraco, G. W. Kling & T. K. Kratz, 1994.
Carbon dioxide supersaturation in the surface waters of
lakes. Science 265: 1568–1570.
Cole, J. J., M. L. Pace, S. R. Carpenter & J. F. Kitchell, 2000.
Persistence of net heterotrophy in lakes during nutrient
addition and food web manipulations. Limnology and
Oceanography 45: 1718–1730.
Cole, J. J., Y. T. Prairie, N. F. Caraco, W. H. McDowell, L.
J. Tranvik, R. G. Striegl, C. M. Duarte, P. Kortelainen, J.
A. Downing, J. J. Middelburg & J. Melack, 2007. Plumbing
the global carbon cycle: integrating inland waters into the
terrestrial carbon budget. Ecosystems 10: 171–184.
Davidson, T. A., J. Audet, J.-C. Svenning, T. L. Lauridsen, M.
Søndergaard, F. Landkildehus, S. E. Larsen & E. Jeppesen,
2015. Eutrophication effects on greenhouse gas fluxes from
shallow lake mesocosms override those of climate warm-
ing. Global Change Biology. doi:10.1111/gcb.13062.
Dean, W. E. & E. Gorham, 1998. Magnitude and significance of
carbon burial in lakes, reservoirs and peatlands. Geology
26: 535–538.
Declerck, S., J. Vandekerkhove, L. S. Johansson, K. Muylaert, J.
M. Conde-Porcuna, K. van der Gucht, T. Lauridsen, K.
Schwenk, G. Zwart, W. Rommens & J. Lopez-Ramos,
2005. Multi-group biodiversity in shallow lakes along
gradients of phosphorus and water plant cover. Ecology 86:
1905–1915.
de Kluijver, A., J. Ning, Z. Liu, E. Jeppesen & J. J. Middelburg,
2015. Macrophyte and periphyton carbon subsidies to
bacterioplankton and zooplankton in a shallow, eutrophic
lake in tropical China. Limnology and Oceanography 60:
375–385.
Downing, J. A., Y. T. Prairie, J. J. Cole, M. Duarte, L. J. Tranvik,
R. G. Striegl, W. H. McDowell, P. Kortelainen, N.
F. Caraco, J. M. Melack & J. J. Middelburg, 2006. The
global abundance and size distribution of lakes, ponds, and
impoundments. Limnology and Oceanography 51:
2388–2397.
Dudgeon, D., A. H. Arthington, M. O. Gessner, Z.-I. Kawabata,
D. J. Knowler, C. Le
´ve
ˆque, R. J. Naiman, A.-H. Prieur-
Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006.
42 Hydrobiologia (2016) 778:33–44
123
Freshwater biodiversity: importance, threats, status and
conservation challenges. Biological Reviews 81: 163–182.
Gao, J., Z. Liu & E. Jeppesen, 2014. Fish trophic structures but
not biomass changed after lake restoration by biomanipu-
lation in a tropical eutrophic lake. Hydrobiologia 724:
127–140.
Genkai-Kato, M., Y. Vadeboncoeur, L. Liboriussen & E.
Jeppesen, 2012. Benthic-pelagic coupling, regime shifts
and whole-lake primary production in shallow lakes.
Ecology 93: 619–631.
Higgins, S. N. & M. J. Vander Zanden, 2010. What a difference
a species makes: a meta-analysis of dreissenid mussel
impacts on freshwater ecosystems. Ecological Monographs
80: 179–196.
Huttunen, J. T., S. Juutinen, J. Alm, T. Larmola, T. Hammar, J.
Silvola & P. J. Martikainen, 2003. Fluxes of methane,
carbon dioxide and nitrous oxide in boreal lakes and
potential anthropogenic effects on the aquatic greenhouse
gas emissions. Chemosphere 52: 609–621.
Idrisi, N., E. L. Mills, L. G. Rudstam & D. J. Stewart, 2001.
Impact of zebra mussels (Dreissena polymorpha) on the
pelagic lower trophic levels of Oneida Lake, New York.
Candian Journal of Fisheries and Aquatic Sciences 58:
1430–1441.
Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen, F.
P. Møller & K. Sandby, 1998. Changes in nitrogen reten-
tion in shallow eutrophic lakes following a decline in
density of cyprinids. Archiv fu
¨r Hydrobiologie 142:
129–151.
Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen & F.
Landkildehus, 2000. Trophic structure, species richness
and biodiversity in Danish lakes: changes along a phos-
phorus gradient. Freshwater Biology 45: 201–213.
Jeppesen, E., M. Søndergaard, T. L. Lauridsen, T. A. Davidson,
Z. Liu & N. Mazzeo, 2012. Biomanipulation as a restoration
tool to combat eutrophication: recent advances and future
challenges. Advances in Ecological Research 47: 411–487.
Jones, J. I., 2005. The metabolic cost of bicarbonate use in the
submerged plant Elodea nuttallii. Aquatic Botany 83:
71–81.
Jones, J. I., K. Hardwick & J. W. Eaton, 1996. Diurnal carbon
restrictions on the photosynthesis of dense stands of Elodea
nuttallii (Planch.) St. John. Hydrobiologia 340: 11–16.
Jones, J. I., J. W. Eaton & K. Hardwick, 2000. The effect of
changing environmental variables in the surrounding water
on the physiology of Elodea nuttallii. Aquatic Botany 66:
115–129.
Karatayev, A. Y., D. K. Padilla, D. Minchin, D. Boltovskoy & L.
E. Burlakova, 2007. Changes in global economies and
trade: the potential spread of exotic freshwater bivalves.
Biological Invasions 9: 161–180.
Kidmose, J., B. Nilsson, P. Engesgaard, M. Frandsen, S. Karan,
F. Landkildehus, M. Søndergaard & E. Jeppesen, 2013.
Focused groundwater discharge of phosphorus to a
eutrophic seepage lake (Lake Væng, Denmark): implica-
tions for lake ecological state and restoration. Hydrogeol-
ogy Journal 2: 1787–1802.
Kling, G. W., G. W. Kipphut & M. C. Miller, 1992. The flux of
CO
2
and CH
4
from lakes and rivers in arctic Alaska.
Hydrobiologia 240: 23–36.
Kosten, S., F. Roland, D. M. L. Da Motta Marques, E. H. Van
Nes, N. Mazzeo, L. D. S. L. Sternberg, M. Scheffer & J.
J. Cole, 2010. Climate-dependent CO
2
emissions from
lakes. Global Biogeochemical Cycles 24: GB2007.
Kronvang, B., G. Ærtebjerg, R. Grant, P. Kristensen, M. Hov-
mand & J. Kirkegaard, 1993. Nation-wide Danish moni-
toring programme – state of the aquatic environment.
Ambio 22: 176–187.
Lauridsen, T., E. Jeppesen & F. Ø. Andersen, 1993. Coloniza-
tion of sub-merged macrophytes in shallow fish manipu-
lated lake Væng: Impact of sediment compo-si-tion and
birds grazing. Aquatic Botany 46: 1–15.
Lauridsen, T. L., E. Jeppesen & M. Søndergaard, 1994. Colo-
nization and succession of submerged macrophytes in
shallow Lake Væng during the first five years following
fish manipulation. Hydrobiologia 275(276): 233–242.
Lauridsen, T. L., J. P. Jensen, E. Jeppesen & M. Søndergaard,
2003. Response of submerged macrophytes in Danish lakes
to nutrient loading reductions and biomanipulation.
Hydrobiologia 506–509: 641–649.
Liboriussen, L. & E. Jeppesen, 2003. Temporal dynamics in
epipelic, pelagic and epiphytic algal production in a clear
and a turbid shallow lake. Freshwater Biology 48:
418–431.
Liboriussen, L., M. Søndergaard & E. Jeppesen (red.), 2007.
Sørestaurering i Danmark. Faglig rapport fra DMU 636:
del I 86 s ?del II 312 s. (in Danish)
Liboriussen, L., T. L. Lauridsen, M. Søndergaard, F. Land-
kildehus, M. Søndergaard & E. Jeppesen, 2011. Climate
warming effect on the seasonal dynamics in sediment
respiration in shallow lakes: an outdoor mesocosms
experiment. Freshwater Biology 56: 437–447.
Marklund, O., H. Sandsten, L.-A. Hansson & I. Blindow, 2002.
Effects of waterfowl and fish on submerged vegetation and
macroinvertebrates. Freshwater Biology 47: 2049–2059.
Mayer, C. M., R. A. Keats, L. G. Rudstam & E. L. Mill, 2002.
Scale-dependent effects of zebra mussels on benthic
invertebrates in a large eutrophic lake. Journal of the North
American Benthological Society 21: 616–633.
Moss, B., 1990. Engineering and biological approaches to the
restoration from eutrophication of shallow lakes in which
aquatic plant communities are important components.
Hydrobiologia 200(201): 367–377.
Moss, B., J. Madgwick & G. L. Phillips, 1996. A Guide to the
Restoration of Nutrient-Enriched Shallow Lakes. Broads
Authority & Environment Agency, Norwich.
Moss, B., S. Kosten, M. Meerhoff, R. W. Battarbee, E. Jeppesen,
N. Mazzeo, K. Havens, G. Lacerot, Z. Liu, L. De Meester,
H. Paerl & M. Scheffer, 2011. Allied attack: climate
change and nutrient pollution. Inland Waters 1: 101–105.
Muylaert, K., C. Pe
´rez-Martı
´nez, P. Sa
´nchez-Castillo, T.
L. Lauridsen, M. Vanderstukken, S. A. J. Declerck, K. Van
der Gucht, J. M. Conde-Porcuna, E. Jeppesen, L. De
Meester & W. Vyverman, 2010. Influence of nutrients,
submerged macrophytes and zooplankton grazing on
phytoplankton biomass and diversity along a latitudinal
gradient in Europe. Hydrobiologia 653: 79–90.
Nielsen, A., D. Trolle, R. Bjerring, M. Søndergaard, J. E. Olesen
& E. Jeppesen, 2014. Effects of climate and nutrient load
on the water quality of shallow lakes assessed through
Hydrobiologia (2016) 778:33–44 43
123
ensemble runs by PCLake. Ecological Applications 24:
1926–1944.
Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem
studies. Annual Review of Ecology and Systematics 18:
293–320.
Prejs, A., 1984. Herbivory by temperate freshwater fishes and its
consequences. Environmental Biology of Fishes 10:
281–296.
Provoost, P., S. van Heuven, K. Soetaert, R. Laane & J.
J. Middelburg, 2010. Long-term record of pH in the Dutch
coastal zone: a major role for eutrophication-induced
changes. Biogeosciences Discussions 7: 4127–4152.
Raymond, P. A., J. Hartmann, R. Lauerwald, S. Sobek, C.
McDonald, M. Hoover, D. Butman, R. Striegl, E. Mayorga,
C. Humborg, P. Kortelainen, H. Durr, M. Meybeck, P.
Ciais & P. Guth, 2013. Global carbon dioxide emissions
from inland waters. Nature 503: 355–359.
Rodrı
´guez-Gallego, L., N. Mazzeo, J. Gorga, M. Meerhoff, J.
Clemente, C. Kruk, F. Scasso, G. Lacerot, J. Garcı
´a&F.
Quintans, 2004. Effects of an artificial wetland with free-
floating plants on the restoration of a hypertrophic sub-
tropical lake. Lake and Reservoir Management 9: 203–215.
Sandby, K. S. & J. Hansen, 2007. Lake Arreskov. In: Libo-
riussen, L., M. Søndergaard, E. Jeppesen (eds) Sørestau-
rering i Danmark. Report from NERI no. 636 (in Danish).
Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss & E.
Jeppesen, 1993. Alternative equilibria in shallow lakes.
Trends in Ecology and Evolution 8: 275–279.
Stallard, R. F., 1998. Terrestrial sedimentation and the carbon
cycle: coupling weathering and erosion to carbon burial.
Global Biogeochemical Cycles 12: 231–257.
Stewart, T. W., J. G. Miner & R. L. Lowe, 1998. Quantifying
mechanisms for zebra mussel effects on benthic macroin-
vertebrates: organic matter production and shell-generated
habitat. Journal of the North American Benthological
Society 17: 81–94.
Stumm, W. & J. J. Morgan, 1996. Aquatic Chemistry. John
Wiley, New York.
Strand, J. A. & S. E. B. Weisner, 2001. Dynamics of submerged
macrophyte populations in response to biomanipulation.
Freshwater Biology 46: 1397–1408.
Strayer, D. L., N. F. Caraco, J. J. Cole, S. Findlay & M. L. Pace,
1999. Transformation of freshwater ecosystems by
bivalves – a case study of zebra mussels in the Hudson
River. Bioscience 49: 19–27.
Søndergaard, M., E. Jeppesen, E. Mortensen, E. Dall, P. Kris-
tensen & O. Sortkjær, 1990. Phytoplankton biomass
reduction after planktivorous fish reduction in a shallow,
eutrophic lake: a combined effect of reduced internal
P-loading and increased zooplankton grazing. Hydrobi-
ologia 200(201): 229–240.
Søndergaard, M., L. Olufsen, T. Lauridsen, E. Jeppesen & T.
Vindbæk Madsen, 1996. The impact of grazing waterfowl
on submerged macrophytes: in situ experiments in a shal-
low eutrophic lake. Aquatic Botany 53: 73–84.
Søndergaard, M., T. L. Lauridsen, E. Jeppesen & L. Bruun,
1998. Macrophyte-Waterfowl Interactions: Tracking a
Variable Resource and the Impact of Herbivory on Plant
Growth. In Jeppesen, E., M. Søndergaard, M. Søndergaard
& K. Christoffersen (eds.), The Structuring Role of Sub-
merged Macrophytes in Lakes, Vol. 131., Ecological
Studies Series Springer, New York: 298–306.
Talling, J. F., 1976. The depletion of carbon dioxide from lake
water by phytoplankton. Journal of Ecology 64: 79–121.
Tranvik, L. J., J. A. Downing, J. B. Cotner, S. A. Loiselle, R.
G. Striegl, T. J. Ballatore, P. Dillon, L. B. Knoll, T. Kutser,
S. Larsen, I. Laurion, D. M. Leech, S. L. McAllister, D.
M. McKnight, J. Melack, E. Overholt, J. A. Porter, Y.
T. Prairie, W. H. Renwick, F. Roland, B. S. Sherman, D.
W. Schindler, S. Sobek, A. Tremblay, M. J. Vanni, A.
M. Verschoor, E. von Wachenfeldt & G. Weyhenmeyer,
2009. Lakes and reservoirs as regulators of carbon cycling
and climate. Limnology and Oceanography 54: 2298–2314.
Trolle, D., P. A. Staehr, T. A. Davidson, R. Bjerring, T.
L. Lauridsen, M. Søndergaard & E. Jeppesen, 2012. Sea-
sonal dynamics of CO
2
flux across the surface of shallow
temperate lakes of contrasting trophic status, and the
response to nutrient load reduction. Ecosystems 15:
336–347.
Vadeboncoeur, Y., E. Jeppesen, M. J. Vander Zanden, H.
H. Schierup, K. Christoffersen & D. Lodge, 2003. From
Greenland to green lakes: cultural eutrophication and the
loss of benthic pathways in lakes. Limnology and
Oceanography 48: 1408–1418.
Vadeboncoeur, Y., G. Peterson, M. J. Vander Zanden & J. Kalff,
2008. Benthic algal productivity across lake size gradients:
interactions among morphometry, nutrients, and light.
Ecology 89: 2542–2552.
Verpoorter, C., T. Kutser, D. A. Seekell & L. J. Tranvik, 2014. A
global inventory of lakes based on high-resolution satellite
imagery. Geophysical Research Letters 41: 6396–6402.
Vo
¨ro
¨smarty, C. J., P. B. McIntyre, M. O. Gessner, D. Dudgeon,
A. Prusevich, P. Green, S. Glidden, S. E. Bunn, C. A. Sul-
livan, C. Reidy Liermann & P. M. Davies, 2010. Global
threats to human water security and river biodiversity.
Nature 467: 555–561.
Wetzel, R. G., 2001. Limnology: Lake and River Ecosystems.
Academic Press, San Diego.
44 Hydrobiologia (2016) 778:33–44
123

Supplementary resource (1)

... This includes the exchange of the greenhouse gases (GHGs) carbon dioxide (CO 2 ) and methane (CH 4 ) with the atmosphere (Aben et al., 2017;Holgerson & Raymond, 2016;Tranvik et al., 2009). Aquatic CO 2 fluxes are strongly influenced by primary production and autotrophic and heterotrophic respiration (Cole et al., 2007;Jeppesen et al., 2016;Larsen et al., 2011;Yang et al., 2015). Methane production and oxidation are conducted by different microorganisms: Archaea mostly produce CH 4 in anoxic and organic matter rich sediments, while aerobic methane-oxidising bacteria (MOB) oxidise CH 4 at the sediment-water interface and in the water column (Bastviken et al., 2008;Biderre-Petit et al., 2011). ...
... Methane produced in the sediments can be released to the atmosphere by diffusion through the water column or by ebullition when bubbles are formed under CH 4 supersaturated conditions (Bastviken et al., 2004). At the ecosystem level, GHG fluxes are therefore determined by the interplay between abiotic factors, such as organic matter and oxygen (O 2 ) availability, and biotic factors such as community structure and trophic interactions (Bastviken et al., 2008;Jeppesen et al., 2016;Palma-Silva et al., 2013). ...
... Fish strongly influence lake carbon processes in various ways. Zooplanktivorous fish, for instance, may reduce largebodied zooplankton densities as to promote phytoplankton growth (Brooks & Dodson, 1965;Hansson et al., 2012), enhancing net primary production and CO 2 fixation (Grasset et al., 2020;Jeppesen et al., 2016;Schindler, 1997). Furthermore, a recent study suggests that zooplanktivores may weaken zooplankton grazing pressure on MOB, resulting in increased MOB biomass (i.e. a trophic cascade) and increased oxidation of CH 4 in the water column (Devlin et al., 2015). ...
Article
Full-text available
• Shallow aquatic systems exchange large amounts of carbon dioxide (CO2) and methane (CH4) with the atmosphere. The production and consumption of both gases is determined by the interplay between abiotic (such as oxygen availability) and biotic (such as community structure and trophic interactions) factors. • Fish communities play a key role in driving carbon fluxes in benthic and pelagic habitats. Previous studies indicate that trophic interactions in the water column, as well as in the benthic zone can strongly affect aquatic CO2 and CH4 net emissions. However, the overall effect of fish on both pelagic and benthic processes remains largely unresolved, representing the main focus of our experimental study. • We evaluated the effects of benthic and pelagic fish on zooplankton and macroinvertebrates; on CO2 and CH4 diffusion and ebullition, as well as on CH4 production and oxidation, using a full-factorial aquarium experiment. We compared five treatments: absence of fish (control); permanent presence of benthivorous fish (common carps, benthic) or zooplanktivorous fish (sticklebacks, pelagic); and intermittent presence of carps or sticklebacks. • We found trophic and non-trophic effects of fish on CO2 and CH4 emissions. Intermittent presence of benthivorous fish promoted a short-term increase in CH4 ebullition, probably due to the physical disturbance of the sediment. As CH4 ebullition was the major contributor to the total greenhouse gas (GHG) emissions, incidental bioturbation by benthivorous fish was a key factor triggering total carbon emissions from our aquariums. • Trophic effects impacted GHG dynamics in different ways in the water column and the sediment. Fish predation on zooplankton led to a top-down trophic cascade effect on methane-oxidising bacteria. This effect was, however, not strong enough as to substantially alter CH4 diffusion rates. Top-down trophic effects of zooplanktivorous and benthivorous fish on benthic macroinvertebrates, however, were more pronounced. Continuous fish predation reduced benthic macroinvertebrates biomass decreasing the oxygen penetration depth, which in turn strongly reduced water–atmosphere CO2 fluxes while it increased CH4 emission. • Our work shows that fish can strongly impact GHG production and consumption processes as well as emission pathways, through trophic and non-trophic effects. Furthermore, our findings suggest their impact on benthic organisms is an important factor regulating carbon (CO2 and CH4) emissions.
... Eutrophication is a paramount environmental concern worldwide (Carpenter et al., 1999;Jeppesen et al., 2012), but its role as a driver of the direction and magnitude of GHG flux from/to lentic ecosystems remains unclear. The role of lakes as sources or sinks of C is highly dependent on the balance between primary production and ecosystem respiration (e.g., Cole et al., 2000;Jeppesen et al., 2016;Prairie et al., 2002). Lakes with high loading of organic C tend to be net heterotrophic ecosystems and act as significant sources of C to the atmosphere through respiration (e.g., Andersson and Sobek, 2006;Hanson et al., 2003;Laas et al., 2012). ...
... The present study included a limited number (n = 11) of gravel pit lakes and a more complete survey is still needed to fully estimate their contribution. This is particularly important to quantify annual emissions of gravel pit lakes since it is likely that benthic and epilimnetic metabolisms as well as resulting gas flux vary between seasons and years (e.g., Jeppesen et al., 2016;Laas et al., 2012). In particular, considering that the magnitude of sediment respiration and the epilimnetic metabolism are strongly regulated by primary production, one might expect a switch from net autotrophy to net heterotrophy during the winter season due to a reduced phytoplankton growth (Marshall and Peters, 1989). ...
Article
Lentic ecosystems play a major role in the global carbon cycling but the understanding of the environmental determinants of lake metabolism is still limited, notably in small artificial lakes. Here the effects of environmental conditions on lake metabolism and CO2 and CH4 emissions were quantified in 11 small artificial gravel pit lakes covering a gradient of ecosystem maturity, ranging from young oligotrophic to older, hypereutrophic lakes. The diffusive fluxes of CO2 and CH4 ranged from −30.10 to 37.78 mmol m−2 d−1 and from 3.05 to 25.45 mmol m−2 d−1 across gravel pit lakes, respectively. Nutrients and chlorophyll a concentrations were negatively correlated with CO2 concentrations and emissions but positively correlated with CH4 concentrations and emissions from lakes. These findings indicate that, as they mature, gravel pit lakes switch from heterotrophic to autotrophic-based metabolism and hence turn into CO2-sinks. In contrast, the emission of CH4 increased along the maturity gradient. As a result, eutrophication occurring during ecosystem maturity increased net emissions in terms of climate impact (CO2 equivalent) due to the higher contribution of CH4 emissions. Overall, mean CO2equivalent emission was 7.9 g m−2 d−1, a value 3.7 and 4.7 times higher than values previously reported in temperate lakes and reservoirs, respectively. While previous studies reported that lakes represent emitters of C to the atmosphere, this study highlights that eutrophication may reverse lake contribution to global C budgets. However, this finding is to be balanced with the fact that eutrophication also increased CH4 emissions and hence, enhanced the potential impact of these ecosystems on climate. Implementing mitigation strategies for maintaining intermediate levels of maturity is therefore needed to limit the impacts of small artificial waterbodies on climate. This could be facilitated by their small size and should be planned at the earliest stages of artificial lake construction.
... 3). Current and expected reduced wind-speed in many parts of the world (atmospheric stilling)(Mölter et al., 2016) will accelerate lake thermal responses to warming and lengthen stratification(Woolway et al., 2019), further enhancing the risk of having low oxygen concentrations at the sediment surface in shallow lakes(Deng et al. 2018) and thus enhancing the risk of higher CH4 emissions.The alternative dominance by phytoplankton, submerged plants, and free-floating vegetation, that are likely under eutrophic conditions, can promote contrasting patterns in CO2 and other GHG fluxesAlmeida et al. 2016;Jeppesen et al. 2016;Audet et al. 2017). While all primary producers take up CO2 through photosynthesis and release CO2 through respiration, the effects on CH4 and N2O dynamics may differ among phytoplankton, submerged, free-floating, or emergent macrophytes. ...
Preprint
Full-text available
NON FORMATED PUBLISHED VERSION Feedbacks between climate change and eutrophication: revisiting the allied attack concept and how to strike back Despite its well-established negative impacts on society and biodiversity, eutrophication continues to be one of the most pervasive anthropogenic influence along the freshwater to marine continuum. The interaction between eutrophication and climate change, particularly climate warming, was explicitly focused upon a decade ago in the paper by Moss et al. (2011), which called for an integrated response to both problems, given their apparent synergy. In this review, we summarise advances in the theoretical framework and empirical research on this issue and analyse the current understanding of the major drivers and mechanisms by which climate change can enhance eutophication, and vice versa, with a particular focus on shallow lakes. Climate change can affect nutrient loading, through changes at the catchment and landscape levels by affecting hydrological patterns and fire frequency, and through temperature effects on nutrient cycling. Biotic communities and their interactions can also be directly and indirectly affected by climate change, leading to an overall weakening of resilience to eutrophication impacts. Increasing empirical evidence now indicates several mechanisms by which eutrophying aquatic systems can increasingly act as important sources of greenhouse gases to the atmosphere, particularly methane. We also highlight potential feedbacks between eutrophication, cyanobacterial blooms, and climate change. Facing both challenges at the same time is more pressing than ever. Meaningful and strong measures at the landscape and water body levels are therefore required if we are to ensure ecosystem resilience and safe water supply, conserving biodiversity, and decreasing the carbon footprint of freshwaters.
... While generally positive, these changes are not free from a downside in terms of ecosystem services. For example, when lakes shift from a turbid to a clear water state the efflux of CO 2 can increase significantly (Jeppesen et al. 2015). ...
Article
The economic costs of non-indigenous species (NIS) are a key factor for the allocation of efforts and resources to eradicate or control baneful invasions. Their assessments are challenging, but most suffer from major flaws. Among the most important are the following: (1) the inclusion of actual damage costs together with various ancillary expenditures which may or may not be indicative of the real economic damage due to NIS; (2) the inclusion of the costs of unnecessary or counterproductive control initiatives; (3) the inclusion of controversial NIS-related costs whose economic impacts are questionable; (4) the assessment of negative impacts only, ignoring the positive ones that most NIS have on the economy, either directly or through their ecosystem services. Such estimates necessarily arrive at negative and often highly inflated values, do not reflect the net damage and economic losses due to NIS, and can significantly misguide management and resource allocation decisions. We recommend an approach based on holistic costs and benefits that are assessed using likely scenarios and their counter-factual.
... 3). Current and expected reduced wind-speed in many parts of the world (atmospheric stilling)(Mölter et al., 2016) will accelerate lake thermal responses to warming and lengthen stratification(Woolway et al., 2019), further enhancing the risk of having low oxygen concentrations at the sediment surface in shallow lakes(Deng et al. 2018) and thus enhancing the risk of higher CH4 emissions.The alternative dominance by phytoplankton, submerged plants, and free-floating vegetation, that are likely under eutrophic conditions, can promote contrasting patterns in CO2 and other GHG fluxesAlmeida et al. 2016;Jeppesen et al. 2016;Audet et al. 2017). While all primary producers take up CO2 through photosynthesis and release CO2 through respiration, the effects on CH4 and N2O dynamics may differ among phytoplankton, submerged, free-floating, or emergent macrophytes. ...
Article
Despite its well-established negative impacts on society and biodiversity, eutrophication continues to be one of the most pervasive anthropogenic influence along the freshwater to marine continuum. The interaction between eutrophication and climate change, particularly climate warming, was explicitly focused upon a decade ago in the paper by Moss et al. (2011), which called for an integrated response to both problems, given their apparent synergy. In this review, we summarise advances in the theoretical framework and empirical research on this issue and analyse the current understanding of the major drivers and mechanisms by which climate change can enhance eutophication, and vice versa, with a particular focus on shallow lakes. Climate change can affect nutrient loading, through changes at the catchment and landscape levels by affecting hydrological patterns and fire frequency, and through temperature effects on nutrient cycling. Biotic communities and their interactions can also be directly and indirectly affected by climate change, leading to an overall weakening of resilience to eutrophication impacts. Increasing empirical evidence now indicates several mechanisms by which eutrophying aquatic systems can increasingly act as important sources of greenhouse gases to the atmosphere, particularly methane. We also highlight potential feedbacks between eutrophication, cyanobacterial blooms, and climate change. Facing both challenges at the same time is more pressing than ever. Meaningful and strong measures at the landscape and water body levels are therefore required if we are to ensure ecosystem resilience and safe water supply, conserving biodiversity, and decreasing the carbon footprint of freshwaters.
... The potentially higher productivity of the warmer systems may indirectly narrow CR by increasing the pelagic δ 13 C signal. Moreover, the CO2 flux between a lake and the atmosphere may be affected by the food web structure [84,85]. A higher phytoplankton biomass due to diminished zooplankton biomass as a consequence of, for example, high fish predation, may enhance the influx of CO2 from the atmosphere and thus enrich the δ 13 C signal of the pelagic biota [84]. ...
Article
Full-text available
Disentangling the effects of climate change on nature is one of the main challenges facing ecologists nowadays. Warmer climates forces strong effects on lake biota for fish, leading to a reduction in size, changes in diet, more frequent reproduction, and stronger cascading effects. Space-for-time substitution studies (SFTS) are often used to unravel climate effects on lakes biota; however , results from continental lakes are potentially confounded by biogeographical and evolutionary differences, also leading to an overall higher fish species richness in warm lakes. Such differences may not be found in lakes on remote islands, where natural fish free lakes have been subjected to stocking only during the past few hundred years. We studied 20 species-poor lakes located in two remote island groups with contrasting climates, but similar seasonality: the Faroe Islands (cold; 6.5 ± 2.8 °C annual average (SD) and the Azores Islands (warm; 17.3 ± 2.9 °C)). As for mainland lakes, mean body size of fish in the warmer lakes were smaller overall, and phytoplankton per unit of phosphorus higher. The δ 13 C carbon range for basal organisms, and for the whole food web, appeared wider in colder lakes. In contrast to previous works in continental fresh waters, Layman metrics of the fish food web were similar between the two climatic regions. Our results from insular systems provide further evidence that ambient temperatures, at least partially, drive the changes in fish size structure and the cascading effects found along latitude gradients in lakes.
Article
Full-text available
The ecosystem services approach to conservation is becoming central to environmental policy decision making. While many negative biological invasion-driven impacts on ecosystem structure and functioning have been identified, much less was done to evaluate their ecosystem services. In this paper, we focus on the often-overlooked ecosystem services provided by three notable exotic ecosystem engineering bivalves, the zebra mussel, the quagga mussel, and the golden mussel. One of the most significant benefits of invasive bivalves is water filtration, which results in water purification and changes rates of nutrient cycling, thus mitigating the effects of eutrophication. Mussels are widely used as sentinel organisms for the assessment and biomonitoring of contaminants and pathogens and are consumed by many fishes and birds. Benefits of invasive bivalves are particularly relevant in human-modified ecosystems. We summarize the multiple ecosystem services provided by invasive bivalves and recommend including the economically quantifiable services in the assessments of their economic impacts. We also highlight important ecosystem disservices by exotic bivalves, identify data limitations, and future research directions. This assessment should not be interpreted as a rejection of the fact that invasive mussels have negative impacts, but as an attempt to provide additional information for scientists, managers, and policymakers.
Article
Full-text available
In this review we describe patterns and mechanisms by which habitat complexity is crucial for the functioning of shallow lakes and ponds, and for the abundance and diversity of biological communities in these ecosystems. Habitat complexity is affected by processes acting at different spatial scales, from the landscape to the ecosystem level (i.e., morphometric attributes) that generate different complexities, determining the potential for organisms to succeed and processes to occur, such as energy and nutrient transfer, and fluxes of greenhouse gases, among others. At the local scale, the three major habitats, pelagic, littoral, and benthic, are characterised by different degrees of structural complexity and a particular set of organisms and processes. Direct and indirect effects of changes in within-lake habitat complexity can either hinder or promote regime shifts in these systems. We also review several anthropogenic pressures (eutrophication, urbanisation, introduction of exotic species, and climate change) that decrease lake resilience through changes in habitat complexity and strategies for habitat complexity restoration. Overall, we emphasize the need to preserve and/or restore habitat complexity as key challenges to account for ecosystem integrity, maintenance of local/regional biodiversity, and for the provision of crucial ecosystem services (e.g., biodiversity, self-purification, and carbon sequestration).
Article
Full-text available
Fluxes of carbon dioxide (CO2) and methane (CH4) in shallow lakes are strongly affected by dominant primary producers which mostly has been studied in temperate and boreal regions. We compared summer CO2 and CH4 fluxes (diffusion and ebullition) in littoral and pelagic zones of three subtropical shallow lakes with contrasting regimes: clear-vegetated, phytoplankton-turbid, and sediment-turbid, and assessed fluxes in different seasons in the clear-vegetated system. Significant differences among the lakes occurred only for CH4 fluxes. In the sediment-turbid lake we found undersaturated CH4 concentrations were below atmospheric equilibrium, implying CH4 uptake (< 0 mg m−2 day−1), likely due to low availability of organic matter. Differences between zones occurred in the clear-vegetated and phytoplankton-turbid lakes, with higher total CH4 emissions in the littoral than in the pelagic zones (mean: 4342 ± 895 and 983 ± 801 mg m−2 day−1, respectively). CO2 uptake (< < 0 mg m−2 day−1) occurred in the littoral of the phytoplankton-turbid lake (in summer), and in the pelagic of the clear-vegetated lake even in winter, likely associated with submerged macrophytes dominance. Our work highlights the key role of different primary producers regulating carbon fluxes in shallow lakes and points out that, also in the subtropics, submerged macrophyte dominance may decrease carbon emissions to the atmosphere.
Article
In mountainous lake areas, lake-land and mountain-valley breezes interact with each other, leading to an “extended lake breeze”. These extended lake breezes can regulate and control energy and carbon cycles at different scales. Based on meteorological and turbulent fluxes data from an eddy covariance observation site at Erhai Lake in the Dali Basin, southwest China, characteristics of daytime and nighttime extended lake breezes and their impacts on energy and carbon dioxide exchange in 2015 are investigated. Lake breezes dominate during the daytime while, due to different prevailing circulations at night, there are two types of nighttime breezes. The mountain breeze from the Cangshan Mountain range leads to N1 type nighttime breeze events. When a cyclonic circulation forms and maintains in the southern part of Erhai Lake at night, its northern branch contributes to the formation of N2 type nighttime breeze events. The prevailing wind directions for daytime, N1, and N2 breeze events are southeast, west, and southeast, respectively. Daytime breeze events are more intense than N1 events and weaker than N2 events. During daytime breeze events, the lake breeze decreases the sensible heat flux (Hs) and carbon dioxide flux (\(\boldsymbol{F}_{\text{CO}_{2}}\)) and increases the latent heat flux (LE). During N1 breeze events, the mountain breeze decreases Hs and LE and increases \(\boldsymbol{F}_{\text{CO}_{2}}\). For N2 breeze events, the southeast wind from the lake surface increases Hs and LE and decreases \(\boldsymbol{F}_{\text{CO}_{2}}\). Results indicate that lakes in mountainous areas promote latent heat mixing but suppress carbon dioxide exchange.
Article
Full-text available
Net ecosystem production (NEP) is the difference between gross primary production (GPP) and community respiration (R). We estimated in situ NEP using three independent approaches (net CO2 gas flux, net O-2 gas flux, and continuous diel O-2 measurements) over a 4-7 yr period in a series of small lakes in which food webs were manipulated and nutrient loadings were experimentally varied. In the absence of manipulation, these lakes were net heterotrophic according to all three approaches. NEP (NEP = GPP-R) was consistently negative and averaged -35.5 +/- 3.7 (standard error) mmol C m(-2) d(-1). Nutrient enrichment, in the absence of strong planktivory, tended to cause increases in estimates of both GPP and R (estimated from the continuous O-2 data) but resulted in little change in the GPP/R ratio, which remained <1, or NEP, which remained negative. When planktivorous fish dominated the food web, large zooplankton were rare and nutrient enrichment produced positive values of NEP by all three methods. Among lakes and years, daily values of NEP ranged from -241 to +175 mmol m(-2) d(-1); mean seasonal NEP was positive only under a combination of high nutrient loading and a planktivore-dominated food web. Community R is significantly subsidized by allochthonous sources of organic matter in these lakes. Combining all lakes and years, we estimate that 26 mmol C m(-2) d(-1) of allochthonous origin is respired on average. This respiration of allochthonous organic matter represents 13 to 43% of total R, and this fraction declines with increasing GPP.
Article
Full-text available
Fresh waters make a disproportionately large contribution to greenhouse gas (GHG) emissions, with shallow lakes being particular hotspots. Given their global prevalence, how GHG fluxes from shallow lakes are altered by climate change may have profound implications for the global carbon cycle. Empirical evidence for the temperature dependence of the processes controlling GHG production in natural systems is largely based on the correlation between seasonal temperature variation and seasonal change in GHG fluxes. However, ecosystem-level GHG fluxes could be influenced by factors, which whilst varying seasonally with temperature are actually either indirectly related (e.g. primary producer biomass) or largely unrelated to temperature, for instance nutrient loading. Here, we present results from the longest running shallow-lake mesocosm experiment which demonstrate that nutrient concentrations override temperature as a control of both the total and individual GHG flux. Furthermore, testing for temperature treatment effects at low and high nutrient levels separately showed only one, rather weak, positive effect of temperature (CH4 flux at high nutrients). In contrast, at low nutrients, the CO2 efflux was lower in the elevated temperature treatments, with no significant effect on CH4 or N2 O fluxes. Further analysis identified possible indirect effects of temperature treatment. For example, at low nutrient levels increased macrophyte abundance was associated with significantly reduced fluxes of both CH4 and CO2 for both total annual flux and monthly observation data. As macrophyte abundance was positively related to temperature treatment, this suggests the possibility of indirect temperature effects, via macrophyte abundance, on CH4 and CO2 flux. These findings indicate that fluxes of GHGs from shallow lakes may be controlled more by factors indirectly related to temperature, in this case nutrient concentration and the abundance of primary producers. Thus, at ecosystem scale response to climate change may not follow predictions based on the temperature dependence of metabolic processes. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Chapter
Submerged macrophytes are important for the maintenance of clear water in shallow eutrophic lakes (Jeppesen et al., 1990; Scheffer, 1990; Hargeby et al., 1994), and establishment of permanent macrophy te coverage is an important aspect of the lake restoration process after a reduction of nutrient loading. However, as macrophytes are subject to grazing by herbivores such as waterfowl (e.g., Lodge, 1991), it may be speculated whether waterfowl grazing can delay recolonization and thereby lake recovery. The impact of waterfowl grazing on macrophytes is poorly documented (Winfield, 1991), and few studies have considered it important, examples being Jupp and Spence (1977), who ascribed growth limitation of Potamogeton filiformis and Potamogeton pectinatus to wave action and waterfowl grazing, and van Donk et al. (1994), who observed that intensive coot herbivory in Lake Zwemlust (up to 120 individuals/ha) affected Elodea biomass and species composition.
Article
This paper examines the linkages between the carbon cycle and sedimentary processes on land. Available data suggest that sedimentation on land can bury vast quantities of organic carbon, roughly 1015 g C yr-1. To evaluate the relative roles of various classes of processes in the burial of carbon on land, terrestrial sedimentation was modeled as a series of 864 scenarios. Each scenario represents a unique choice of intensities for seven classes of processes and two different global wetland distributions. Comparison was made with presumed preagricultural conditions. The classes of processes were divided into two major component parts: clastic sedimentation of soil-derived carbon and organic sedimentation of autochthonous carbon. For clastic sedimentation, masses of sediment were considered for burial as reservoir sediment, lake sediment, and combined colluvium, alluvium, and aeolian deposits. When the ensemble of models is examined, the human-induced burial of 0.6-1.5.1015 g yr-1 of carbon on land is entirely plausible. This sink reaches its maximum strength between 30 ° and 50°N. Paddy lands stand out as a type of land use that warrants future study, but the many faces of rice agriculture limit generalization. In an extreme scenario, paddy lands alone could be made to bury about 1.1015 g C yr-1. Arguing that terrestrial sedimentation processes could be much of the sink for the so called 'missing carbon' is reasonable. Such a hypothesis, however, requires major redesign of how the carbon cycle is modeled. Unlike ecosystem processes that are amenable to satellite monitoring and parallel modeling, many aspects of terrestrial sedimentation are hidden from space.
Article
Protecting the worlds freshwater resources requires diagnosing threats over a broad range of scales, from global to local. Here we present the first worldwide synthesis to jointly consider human and biodiversity perspectives on water security using a spatial framework that quantifies multiple stressors and accounts for downstream impacts. We find that nearly 80% of the worlds population is exposed to high levels of threat to water security. Massive investment in water technology enables rich nations to offset high stressor levels without remedying their underlying causes, whereas less wealthy nations remain vulnerable. A similar lack of precautionary investment jeopardizes biodiversity, with habitats associated with 65% of continental discharge classified as moderately to highly threatened. The cumulative threat framework offers a tool for prioritizing policy and management responses to this crisis, and underscores the necessity of limiting threats at their source instead of through costly remediation of symptoms in order to assure global water security for both humans and freshwater biodiversity.
Article
The monitoring program covers all aquatic media and provides spatial and temporal information on the land-use related distribution of nutrients and their effects on the aquatic environment. Results obtained during the first year are presented together with long-term trends in nutrient loading and surface-water quality. Nitrogen has been documented to be the limiting nutrient for phytoplankton production in Danish marine waters, except in many inshore waters for a short period in spring where phosphorus is the limiting nutrient. One of the main objectives is therefore to reduce nitrogen loading of the aquatic environment by 50% before 1994. -from Authors
Article
To study how changes in biomass of cyprinids (mainly roach, Rutilus rutilus L., and bream, Abramis brama L.) affect nitrogen retention in shallow lakes, we conducted mass balances of total nitrogen for 6-11 years in four eutrophic lakes in which the fish biomass changed markedly, either from natural causes or due to manipulation. The decline in cyprinids led to a shift from a turbid to a clearwater state in three of the four lakes. In these lakes total nitrogen (N) concentrations decreased and the percentage of N retained in the sediment, or lost by denitrification (N(ret)%) increased substantially. In Lake Vaeng, summer N(ret)% increased from 22-39% before to 60-72% after the biomass of cyprinids had been reduced by 50%. N(ret)% temporarily decreased to 42% during a short-term return to the turbid state. In Lake Engelsholm, a 90% reduction in cyprinids resulted in an increase in summer mean N(ret)% from 13-50% to 58-60%, and in Lake Arreskov the annual mean N(ret)% increased from -4-34% before a major fish kill to 54-59% after. A comparison with data from 16 non-manipulated lakes revealed that these changes could not be ascribed to natural interannual variations. No significant changes in N concentrations or N(ret)% were found in Lake Sobygard, which remained turbid and maintained a relatively high biomass of cyprinids. In the three lakes that shifted to a clearwater state, N(ret)% was significantly inversely related to chlorophyll-a, but independent of the abundance of submerged macrophytes and biomass of N-fixing cyanobacteria. The increase in N(ret)% might have resulted from 1) a decrease in organic N in the lake and the outlet due to the decrease in phytoplankton biomass and thus phytoplankton-N, which was not compensated by an increase in inorganic N, 2) reduced resuspension, probably reflecting both a decrease in the number of fish foraging in the sediment and a suggested increase in benthic algal growth, 3) higher denitrification in the sediment, reflecting less competition between denitrifiers and phytoplankton for nitrate, enhanced N retention by phyto- and zoobenthos and enhanced sediment nitrification due to higher oxygen concentrations, the latter reflecting lower sedimentation, higher density of zoobenthos and higher oxygen production by benthic algae. More research is needed to elucidate the relative importance of these mechanisms. It may, however, be concluded that fish manipulation or phosphorus-loading reduction leading to a shift from a turbid to a clearwater state in eutrophic lakes may markedly enhance lake N(ret)% and consequently reduce the transfer of nitrogen to coastal waters.