Science of the Total Environment 768 (2021) 144582

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Science of the Total Environment

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

Review

The role of freshwater eutrophication in greenhouse gas emissions:

A review
Yi Li a, Jiahui Shang a, Chi Zhang b,⁎, Wenlong Zhang a, Lihua Niu a, Longfei Wang a, Huanjun Zhang a
a
Key Laboratory of Integrated Regulation and Resource Development on Shallow Lakes, Ministry of Education, College of Environment, Hohai University, Nanjing 210098, PR China
b
College of Mechanics and Materials, Hohai University, Xikang Road #1, Nanjing 210098, PR China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Role of freshwater eutrophication on

greenhouse gas emissions was
reviewed.
• Significance of freshwater as a source of
greenhouse gases was quantitatively
stated.
• Factors affecting greenhouse gas emis-
sions from eutrophic freshwaters were
analyzed.
• Feedback loops between freshwater eu-
trophication and gas emissions were
emphasized.

a r t i c l e i n f o a b s t r a c t

Article history: Greenhouse gases (GHGs) have long received public attention because they affect the Earth's climate by produc-
Received 5 October 2020 ing the greenhouse effect. Freshwaters are an important source of GHGs, and the enhancement in their eutrophic
Received in revised form 12 December 2020 status affects GHG emissions. Along with the increasing eutrophication of water bodies, the relevant quantitative
Accepted 12 December 2020
and qualitative studies of the effects of freshwater eutrophication on GHG emissions have made substantial prog-
Available online 9 January 2021
ress, particularly in the past 5 years. However, to our knowledge, this is the first critical review to focus on the role
Editor: Jay Gan of freshwater eutrophication in GHG emissions. In this review, the emissions of common GHGs from freshwater
are quantitatively described. Importantly, direct (i.e., dissolved oxygen, organic carbon, and nutrients) and indi-
Keywords: rect factors (i.e., dominant primary producer and algal blooms) affecting GHG emissions from eutrophic freshwa-
Greenhouse gas emissions ter are systematically analyzed. In particular, the existence and significance of feedback loops between
Freshwater eutrophication freshwater eutrophication and GHG emissions are emphasized considering the difficulties managing freshwater
Influencing factors ecosystems and the Earth's climate. Finally, several future research directions as well as mitigation measures are
Feedback loops described to provide useful insight into the dynamics and control of GHG emissions.
© 2021 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1.1. Impact of greenhouse gas emissions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1.2. Role of freshwaters in greenhouse gas emissions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Greenhouse gas emissions from freshwaters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

⁎ Corresponding author.
E-mail address: zhangchi.hhu@qq.com (C. Zhang).

https://doi.org/10.1016/j.scitotenv.2020.144582
0048-9697/© 2021 Elsevier B.V. All rights reserved.
Y. Li, J. Shang, C. Zhang et al. Science of the Total Environment 768 (2021) 144582

3. Direct effects of freshwater eutrophication on greenhouse gas emissions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

3.1. Oxygen content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.2. Organic matter . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.3. Nutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4. Indirect effects of freshwater eutrophication on greenhouse gas emissions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4.1. Shift in the dominant primary producer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.2. Facilitation of harmful algal blooms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5. Feedback loops between freshwater eutrophication and greenhouse gas emissions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
6. Conclusions and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Declaration of competing interest. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

1. Introduction
1.1. Impact of greenhouse gas emissions
Greenhouse gases, including carbon dioxide (CO2), methane (CH4),
and nitrous oxide (N2O), enhance the greenhouse effect by absorbing
and re-emitting energy in the low atmosphere (Montzka et al., 2011).
Large amounts of GHG emissions will alter the Earth's climate and im-
pair natural ecosystems, bringing significant socioeconomic loss
(Dottori et al., 2018; Montzka et al., 2011). Specifically, CO2 is the
most emitted and the most common GHG. CH4 is the second most com-
mon GHG and is 34-times more potent as a GHG than CO2 on a 100-year
time-scale (IPCC, 2013). CH4 emissions have been rising in past decades,
making a growing contribution to global warming (Saunois et al., 2016).
The global warming potential of N2O is 298-times higher than that of
CO2 on a 100-year time-scale (IPCC, 2013), while its low emissions
have attracted relatively less attention (Kumar et al., 2019). In general,
these three common GHGs have different global warming potentials
as well as emission magnitudes, playing important roles in the green-
house effect.
1.2. Role of freshwaters in greenhouse gas emissions
It is obvious that the recognition of the major sources of GHGs ben-
efits a full understanding of the global GHG budget and efficacious im-
plementation measures to control GHG emissions. Freshwaters
(i.e., streams, rivers, lakes, and reservoirs) are considered as a main
source of GHG emissions. CO2 and CH4 emissions from freshwaters are
significant because of the large amounts of organic matter in bodies of
water and sediments (Ortiz-Llorente and Alvarez-Cobelas, 2012;
Raymond et al., 2013), while N2O emissions are much lower than
those of CO2 or CH4, unless considerable nitrogen reaches the freshwa-
ter bodies (Kumar et al., 2019). It has been estimated that the emissions
of CO2, CH4, and N2O from freshwaters are 1.36 (Tranvik et al., 2009),
0.96 (Bastviken et al., 2011), and 0.10 Pg C yr−1 (CO2-equivalents) re-
spectively (Soued et al., 2015). Surprisingly, the sum of these GHG emis-
sions from freshwaters approach to 31% of the annual CO2 emissions
from fossil fuel combustion (7.8 Pg C-CO2 yr−1) (IPCC, 2013). That is
to say, freshwaters are an important location for biogeochemical pro-
cesses that contribute significantly to the global GHG budget.
With the rapid socioeconomic development, increases in the human
population, and climate change, a growing number of bodies of fresh-
waters are becoming eutrophic (Caraco and Cole, 1999; Jeppesen
et al., 2009). It should be noted that eutrophication greatly affects
GHG emissions from freshwaters. Lakes with agricultural catchments
release greater CO2 and CH4 into the air compared with lakes away
from human activities (Huttunen et al., 2003) Many studies have subse-
quently confirmed this phenomenon by showing that eutrophic status,
as indicated by concentrations of chlorophyll a (chl a) and nutrients in
freshwaters, are a major driver of local freshwater GHG emissions
(Lapierre et al., 2017; West et al., 2016; Yang et al., 2015; Yvon-
Durocher et al., 2011). Attractively, the studies that assembled global
datasets of aquatic GHG fluxes and their local drivers have suggested
that trophic status is not only a local but also a major global driver of
GHG emissions from freshwaters (Deemer et al., 2016; Del Sontro
et al., 2019). In particular, CH4 emissions have been observed to rise ex-
ponentially with the concentrations of chl a (Del Sontro et al., 2019).
Nevertheless, other studies have reported that freshwater eutrophica-
tion reduces CO2 emissions by intense photosynthesis (Vachon et al.,
2020), and this reduction might lead to a decrease in net overall GHG
emissions (Grasset et al., 2020). Freshwater eutrophication seriously
threatens water quality and also affects GHG emissions; thus, the role
of freshwater eutrophication in GHG emissions should be attracting in-
creasing scientific concern.
Until now, the unidirectional effects of GHG emissions on climate
change (Montzka et al., 2011) and thus on freshwater eutrophication
(Jeppesen et al., 2010) as well as its associated symptoms (Ficke et al.,
2007; Paerl and Paul, 2012) have been well reviewed. However, there
is still a lack of critical review with regard to the reverse effects of fresh-
water eutrophication on GHG emissions. This topic has recently
attracted increased attention, and explorations of the complex link be-
tween GHG emissions and the eutrophic status of freshwaters are in-
creasing (Beaulieu et al., 2019; Grasset et al., 2020; Sepulveda-Jauregui
et al., 2018; Vachon et al., 2020). Unfortunately, there is still a lack of
comprehensive understanding of various key factors that affect GHG
emissions derived from freshwaters. This knowledge gap is what in-
spired us to critically review the role of freshwater eutrophication in
GHG emissions. Here, we have quantitatively described the importance
of freshwaters as an important source of GHGs and discussed both the
direct and indirect factors affecting GHG emissions from eutrophic
freshwaters. We have also highlighted the existence and significance
of feedback loops between freshwater eutrophication and GHG emis-
sions. We hope that this review will be helpful for scientists and man-
agers who assess the global dynamics of aquatic GHG fluxes and
implement mitigation measures to effectively alleviate the effects of
both freshwater eutrophication and GHG emissions.
2. Greenhouse gas emissions from freshwaters
Freshwaters, including streams, rivers, lakes, and reservoirs have
been considered as one of the substantial sources of GHGs (Bastviken
et al., 2011; Raymond et al., 2013; Soued et al., 2015). Many studies
have identified the important local drivers to better understand the
global dynamics of freshwater GHGs (Huttunen et al., 2003; Lapierre
et al., 2017; West et al., 2016). Importantly, recent advances in technol-
ogy and methods have suggested that several local drivers are factually
global drivers of freshwater GHG fluxes, such as the concentrations of
chl a and nutrients (Deemer et al., 2016; Del Sontro et al., 2019). This
finding has not only improved the accuracy of estimating global fresh-
water GHG fluxes but also highlighted the importance of freshwater

2
Y. Li, J. Shang, C. Zhang et al. Science of the Total Environment 768 (2021) 144582

The mean annual GHG fluxes from main freshwaters with the consideration of the effects of eutrophication. Method types are classified as model prediction of global GHG fluxes (M), global synthesis of local GHG fluxes (G), field observation (F) and
eutrophication on GHG emissions because the concentrations of chl a

Del Sontro et al. (2019)

Huttunen et al. (2003)

Huttunen et al. (2003)

Davidson et al. (2018)

Beaulieu et al. (2019)
and nutrients are key indicators of aquatic eutrophic states. As a result,

Deemer et al. (2016)

Zhou et al. (2020)

comprehensive and process-based knowledge is needed to better un-

Palma-Silva et al.
derstand the role of freshwaters and their eutrophic states in GHG
emissions.

Reference

(2013)
The three most common GHGs, namely CO2, CH4, and N2O, play im-
portant roles in inducing the greenhouse effect and altering the Earth's
climate. In freshwaters, CO2 and CH4 are produced primarily via degra-

Difference

+21,986%
dation of organic matter through aerobic and anaerobic processes, re-

+1738%
+250%

+357%

+108%
(total)

+26%

+50%

+39%
spectively (Kumar et al., 2019). N2O is primarily produced through
microbially mediated nitrification and denitrification (Galloway et al.,
2008). GHGs are emitted from the freshwaters to the atmosphere

1462.8 g m−2 yr−1

4115.8 g m−2 yr−1

417.6 g m−2 yr−1

166.8 g m−2 yr−1

232.2 g m−2 yr−1

626.2 g m−2 yr−1

219.8 g m−2 yr−1

18.6 g m−2 yr−1

34.1 g m−2 yr−1

48.0 g m−2 yr−1

Total (C-CO2eq)b
through four different pathways: diffusion, plant-mediated transport,

3.3 g m−2 yr−1

6.8 g m−2 yr−1
ebullition, and degassing (Bastviken et al., 2004; Kumar et al., 2019;

1.9 Pg yr−1
2.4 Pg yr−1

1.4 Tg yr−1
2.1 Tg yr−1
Tranvik et al., 2009). Diffusion is a common pathway by which GHGs
cross the water-air interface (Bastviken et al., 2004). Plant-mediated
transport involves the movement of GHGs through the stems of emer-

The total annual GHG emissions in CO2-equivalents were calculated using a 34-times conversion factor for CH4 and a 298-times conversion factor for N2O over a 100-yr time-scale.
gent plants from sediments where they are released directly into the at-

Difference
(N2O-N)
mosphere (Bastviken et al., 2004; Tranvik et al., 2009). Ebullition, also

−120%
+230%
+19%

+43%
called bubbling, is a depth-dependent process, and is the primary path-

–
way for the emissions of GHGs with minimal solubility (i.e., CH4) to the

156.43 mg m−2 yr−1

47.45 mg m−2 yr−1

12.06 mg m−2 yr−1

26.57 mg m−2 yr−1

13.57 mg m−2 yr−1

air (Boudreau et al., 2005). Degassing from dam turbines and spillways

9.50 mg m−2 yr−1

is a major pathway for GHG emissions from reservoirs (Deemer et al.,

0.36 Tg yr−1a
2016). These four pathways differ in their implications for transporting

0.30 Tg yr−1
GHGs, but all of them greatly contribute to GHG emissions from

N2O-N
freshwaters.
Different sources of freshwater vary in their contribution to GHG

–
–

–
–
–
–

–
–
emissions. Running water, such as streams and rivers, with a flux of Difference

+48,833%
550 Tg C yr−1 (Cole et al., 2007; Tranvik et al., 2009) acts as an impor-

+1738%

+1739%
(CH4-C)

+398%

+552%

+108%
+31%

+49%
tant source of CO2 emissions, while CH4 emissions are almost negligible
from streams and rivers. Lakes and reservoirs are lentic bodies of fresh-

104,465 mg m−2 yr−1

321,492 mg m−2 yr−1

waters that are the main sources of CH4 (Deemer et al., 2016; Del Sontro

20,964 mg m−2 yr−1

50,648 mg m−2 yr−1

11,678 mg m−2 yr−1

6285 mg m−2 yr−1

2756 mg m−2 yr−1

et al., 2019) with a flux of 91.6 Tg CH4-C yr−1. Specifically, shallow lakes

964 mg m−2 yr−1

657 mg m−2 yr−1

635 mg m−2 yr−1

266 mg m−2 yr−1

552 mg m−2 yr−1
release significantly greater amounts of CH4 than deeper lakes. On the
147 Tg yr−1a
112 Tg yr−1

112 Tg yr−1
167 Tg yr−1

one hand, methanogenesis is promoted due to the high carbon input

into the lake littoral zone (Zhu et al., 2016). On the other hand, CH4
CH4-C

emissions are stimulated due to the sensitivity of shallow lakes to the ef-
fect of differences in atmospheric pressure on the escape of bubbles and
Difference

the short migration distance from the sediment to the water surface
+1240%
(CO2-C)

(Zhu et al., 2016). The differences in CH4 and CO2 emissions between
+89%
−1%

−1%
+7%

running and lentic freshwaters may be due to the different sediment

–

–
types as well as accumulation rates (Maeck et al., 2013). N2O emissions
152,366 mg m−2 yr−1
151,243 mg m−2 yr−1
153,300 mg m−2 yr−1
151,110 mg m−2 yr−1

140,956 mg m−2 yr−1

10,512 mg m−2 yr−1

38,982 mg m−2 yr−1

73,694 mg m−2 yr−1

from freshwaters are much lower than those of CO2 or CH4 and thus are
thought to have a small effect (Del Sontro et al., 2019). Soued et al.
538 Tg yr−1a

(2015) suggested that some pristine boreal freshwater networks act

503 Tg yr−1

as net N2O sinks. Annual GHG emissions from freshwaters are estimated
The number was estimated based on the percentage in the reference.
CO2-C

to be approximately 2.42 Pg C-CO2 eq (Bastviken et al., 2011; Soued

et al., 2015; Tranvik et al., 2009). However, much uncertainty is associ-
–
–

–
–

–
–

ated with these GHG flux estimates, which are based on the traditional
upscaling approach by merely extrapolating the regional biased average
Future (+5 μg L−1

Future (×1.7 chla)

emission rates to the global surface area of freshwaters (Del Sontro

Non-eutrophic

Non-eutrophic

Non-eutrophic

Non-eutrophic

Non-eutrophic

Non-eutrophic

et al., 2019).
Trophic state

To reduce the uncertainties in the GHG flux estimates, researchers

Eutrophic

Eutrophic

Eutrophic

Eutrophic

Eutrophic

Eutrophic
Current

Current

have begun to seek the environmental covariates of GHG emissions

chla)

and adopt alternative upscaling approaches. Some local drivers regulat-

ing GHG emissions from freshwaters, such as chl a and nutrients, have
been identified (Lapierre et al., 2017; West et al., 2016). At the same
Experimental lakes

time, global chl a concentration data can be easily accessed due to recent
Freshwater type

impoundments

impoundments

advances in remote sensing (Sayers et al., 2015). Using the global chl a
Shallow lakes

Shallow lakes
laboratory experiment (E).

and nutrient datasets, along with more than 8000 GHG flux measure-
Reservoirs
reservoirs
Lakes and

Lakes and

ments, Del Sontro et al. (2019) reported that trophic status is a robust
Lakes

driver of lake and reservoir GHG emissions, and concluded that the tra-
ditional upscaling approach underestimates both CH4 and total GHG
Method

emissions. Importantly, lakes and reservoirs with an additional

Table 1

5 μg L−1 chl a are capable of increasing GHG emissions by 0.5 Pg C-

type

E
F

CO2-eq yr−1 (Table 1), which is equivalent to 6.4% of CO2 emissions

b
a

3
Y. Li, J. Shang, C. Zhang et al.
from fossil fuel combustion (IPCC, 2013). Consequently, the significance
of lake and reservoir eutrophication in GHG emissions has been re-
ported; however, there is still a general lack of knowledge of the quan-
titative effect of river and stream eutrophication on GHG emissions.
Many studies have observed that GHG fluxes are affected by the tro-
phic status of the freshwaters (Davidson et al., 2018; Deemer et al.,
2016; Del Sontro et al., 2019; Zhou et al., 2020). The quantitative effects
of freshwater eutrophication on the emissions of different GHGs are
summarized in Table 1, and the detailed calculation information is listed
in the Supplementary Material. Researchers seem to have reached an
agreement that eutrophic freshwaters release significantly more CH4
than non-eutrophic freshwaters. Attractively, it has been estimated
that eutrophic shallow lakes emit 48,833% more CH4 than their non-
eutrophic counterparts (Table 1). This phenomenon is attributed to
the nonlinear or even exponential relationship between CH4 emissions
and freshwater trophic status (Del Sontro et al., 2019; Zhou et al.,
2020). Some researchers have suggested that freshwaters can turn
into CO2 sinks with increases in aquatic primary productivity (Balmer
and Downing, 2011; Grasset et al., 2020; Pacheco et al., 2014), while
others held the opposite opinion and argued that CO2 flux from fresh-
waters is promoted by eutrophication (Zhou et al., 2020), calling for fu-
ture studies to address this divergence. Relatively less attention has
been paid to N2O emissions from freshwaters compared to that of either
CO2 or CH4 emissions. However, the effect of N2O on total GHG fluxes in-
crease with N inputs into freshwaters (Soued et al., 2015; Yang et al.,
2015). As a result, it is necessary to investigate the net effect of freshwa-
ter eutrophication on overall GHG emissions rather than only the bal-
ance between CO2 and CH4 emissions.
3. Direct effects of freshwater eutrophication on greenhouse gas
emissions
Eutrophication is pervasive in many bodies of waters, including
freshwaters and seawaters, often leading to the water quality degrada-
tion (Le Moal et al., 2019). Eutrophication refers to the process of over-
production of organic matter induced by nutrients, primarily N and P
(Ferreira et al., 2011; Le Moal et al., 2019; Smith et al., 1999). Many stud-
ies have shown a significant relationship between freshwater
Fig. 1. Direct effects of freshwater eutrophication on Greenhouse gas emissions. Abundant, high-quality organic matter, low concontrations of dissolved oxygen (DO), and abundant
nitrogen (N) are abiotic traits or conditions associated with eutrophic freshwaters, which will directly affect GHG emissions from the water column.
4
Science of the Total Environment 768 (2021) 144582
eutrophication and GHG emissions (Huttunen et al., 2003; West et al.,
2016), which was directly attributed to the role of abiotic factors
(i.e., oxygen content, organic matter, and nutrients) in the GHG emis-
sions (Fig. 1). Abiotic factors here refer to traits or conditions associated
with eutrophic freshwater. The summary of the effects of abiotic factors
on GHG emissions provides an explicit understanding of the role of
freshwater eutrophication in GHG emissions.
3.1. Oxygen content
Low concentrations of dissolved oxygen (DO) in bottom water and
sediment pore-water are an important characteristic of eutrophic fresh-
waters because of the sinking and decomposition of excess organic matter
(Deemer et al., 2016; Hilton et al., 2006). This oxygen-deficient condition
benefits CH4 production and emissions (Jacinthe et al., 2012; West et al.,
2016) because CH4 is the dominant product of organic carbon mineraliza-
tion under anaerobic conditions (Liikanen et al., 2002). Methanogenesis is
promoted, favoring the formation of CH4 bubbles and thus increasing eb-
ullition flux of CH4 if organic carbon is adequate in the sediments (West
et al., 2016). In addition, algal blooms in eutrophic freshwaters will rap-
idly exhaust oxygen, reduce the rate of CH4 oxidation, and increase the
diffusive flux of CH4 (Yan et al., 2017). Nevertheless, low DO conditions
are likely to benefit overall CH4 emissions.
In addition, CO2 emissions likely increase with a decrease in oxygen
content, as oxygen consumption is accompanied by CO2 production
through organic carbon mineralization (Li et al., 2018). N2O emissions
probably decrease under an oxygen-deficient condition. Bodies of fresh-
waters with low DO concentrations act as N2O sinks (Soued et al., 2015),
resulting from the reducing condition created by anoxic and anaerobic
zones in the bottom water and sediments favoring N2O consumption.
Consequently, CH4 and CO2 emissions are projected to increase, while
N2O emissions have the opposite trend under an oxygen-deficient
condition.
3.2. Organic matter
Chl a is an important indicator of freshwater eutrophication and pro-
ductivity, and its positive relationship with GHG fluxes reflects the
Y. Li, J. Shang, C. Zhang et al. Science of the Total Environment 768 (2021) 144582

effects of organic matter in eutrophic freshwaters on GHG emissions.
Highly productive freshwaters have abundant organic matter. Organic
material settles to the sediment where it is degraded to favor GHG pro-
duction and emissions (Whiting and Chanton, 1993; Yang et al., 2015).
This phenomenon occurs because CO2 and CH4 are the primary final
gaseous products of organic matter mineralization (Duc et al., 2010;
Yvon-Durocher et al., 2011). In addition, the settled organic substrates
fuel the growth of heterotrophs, which accelerates decomposition of or-
ganic matter; therefore, promoting GHG production and emissions (Yan
et al., 2019).
Importantly, freshwater eutrophication not only increases the quan-
tity but also the quality of organic substrates for producing GHGs, partic-
ularly CH4. For example, autochthonous primary production arising
from freshwater nutrient inputs constitutes high-quality substrates.
These high-quality organic substrates are degraded more easily than al-
lochthonous organic substrates; thus, more CH4 is produced due to the
stimulation of oxygen consumption and anaerobic decomposition of or-
ganic matter (Huttunen et al., 2003; West et al., 2016). Considering the
strong association between CH4 production and emissions, more CH4 is
projected to be emitted from freshwaters (West et al., 2016). CO2 emis-
sions are likely to decrease, which is partially attributed to the strength-
ened conversion of organic carbon to CH4 in eutrophic freshwaters
(Moss, 2011). Whether the reduction in CO2 emissions will be offset
by increased emissions of other GHGs remains controversial (Grasset
et al., 2020; Vachon et al., 2020), and further studies are needed to quan-
tify the net effects of freshwater eutrophication on GHG emissions.
3.3. Nutrients
Nutrients are another major abiotic factor affecting GHG emissions,
and the most important direct effect of nutrients is to provide abundant
N in favor N2O production. N2O from freshwaters has received little at-
tention because of its low emissions (Kumar et al., 2019), although it has
the greatest potential to contribute to global warming among the three
GHGs (IPCC, 2013). Nevertheless, enhanced inputs of dissolved inor-
ganic nitrogen (DIN) to freshwaters increase N2O emissions (Baron
et al., 2012; Beaulieu et al., 2010; Seitzinger et al., 2000; Yang et al.,
2015). Soued et al. (2015) reported that some bodies of freshwaters
shift from N2O sinks to N2O sources with increased N loading from an-
thropogenic disturbances. Importantly, the inputs of DIN are projected
to grow due to increased industrial and agricultural use of N
(Galloway et al., 2008; Wang et al., 2020).
In addition, freshwater eutrophication is related not only to nutrient
inputs but also to nutrient imbalances (El-Shehawy et al., 2012; Ferreira
et al., 2011; Glibert, 2020). The N/P ratio in eutrophic freshwaters in-
creases because of the higher removal efficiency of P than N during
wastewater treatment (Tong et al., 2020) and the increased use of N fer-
tilizer compared with P fertilizer in agriculture (Glibert et al., 2014). This
upward trend in the N/P ratio facilitates N2O production and emissions
(Kumar et al., 2017). Accordingly, the nutrient imbalance between N
and P can affect freshwater N2O emissions; thus, there is a need to de-
fine a proper N/P ratio to effectively reduce N2O flux while ensuring
that freshwater eutrophication is not exacerbated.
4. Indirect effects of freshwater eutrophication on greenhouse gas
emissions
Indirect effects refer to the effects of biotic factors on GHG emissions.
These biotic factors, including the dominant primary producer (Fig. 2)
and harmful algal blooms (HABs) (Fig. 3) have relatively complex asso-
ciations with freshwater GHG fluxes. These factors are some of the di-
rect factors mentioned in Section 3, consequently facilitating GHG
emissions from eutrophic freshwaters. The changes in these factors in-
duced by freshwater eutrophication impact GHG emissions. A summary
of indirect effects can provide deeper insight into why freshwater eutro-
phication stimulates GHG emissions from the prospective of biotic

Fig. 2. Effects of a macrophyte-dominant water regime on CH4 and CO2 migration and emissions. Sufficient dissolved oxygen and habitats for methanotrophic bacteria provided by
macrophytes will efficiently reduce methanogenesis rates. After being produced, CH4 can be emitted into the air by three pathways—diffusion, ebullition and plant-mediated transport
—and is more likely to be partly oxidized during migration processes. Unlike emergent plants transporting CH4 directly to the air, submerged plants can transport CH4 to the water so
that part CH4 can be oxidized by methanotrophs, thereby reducing CH4 emissions more effectively.

5
Y. Li, J. Shang, C. Zhang et al. Science of the Total Environment 768 (2021) 144582

Fig. 3. Conceptual diagram of the effects of harmful algal blooms (HABs) on greenhouse gas (GHG) emissions. HABs can facilitate GHG emissions in both direct and indirect pathways. In the
direct pathway (indicated in blue), algae accumulated during HABs can directly reduce CO2 emissions and increase CH4 and N2O emissions because of their ability to consume CO2 and
produce CH4 and N2O. At the same time, dense scums will be formed, preventing reoxygenation processes and thus favor CH4 emissions. A large amount of algal-derived organic
carbon will be released from the decomposed algae. The large addition of algal-derived carbon will stimulate the co-metabolic effects of mixed organic substrates and thus favor CO2
and CH4 emissions. In the indirect pathway (indicated in yellow), nutrient released from both decomposed algae and sediments will stimulate freshwater eutrophication, thus
affecting GHG emissions.

processes, benefiting management agencies to adopt effective mitiga-
tion measures.
4.1. Shift in the dominant primary producer
Submerged plants are the dominant primary producer in oligotro-
phic freshwaters (Hilton et al., 2006), and they are gradually replaced
by other aquatic macrophytes or algae when nutrient loading crosses
a critical threshold (Scheffer et al., 1993). A classic example of this phe-
nomenon is the shift from a clear, macrophyte-dominated regime to-
wards a turbid, phytoplankton-dominated regime in a shallow lake
driven by nutrient inputs (Gsell et al., 2016; Scheffer et al., 1993). Im-
portantly, this shift in the dominant primary producer is self-
strengthened by a vicious cycle—fewer macrophytes → more
algae → more turbidity → fewer macrophytes, and so on (Dakos et al.,
2019), which makes the recovery of a clear state in a shallow lake
even more difficult (Su et al., 2019). Consequently, the increase in eutro-
phic status of freshwaters is accompanied by decreased diversity/abun-
dance of aquatic macrophyte species.
A shift in the dominant primary producer partially affects GHG emis-
sions from freshwaters because submerged plants effectively reduce
CH4 emissions for three reasons (Fig. 2). First, macrophytes enhance
the activity of methanotrophic bacteria reducing methanogenesis by
delivering oxygen to the sediments (Ai et al., 2019; Sorrell et al.,
2002). Second, the surfaces of macrophytes provide suitable habitats
for methanotrophic bacteria, which benefit CH4 oxidation (Heilman
and Carlton, 2001). Specifically, CH4 oxidation on the surface of sub-
merged plants is greater than that of emergent plants (Yoshida et al.,
2014). Third, submerged plants transport CH4 to the water column
where it is partially oxidized and diffuses across the water-air interface
(Sanders et al., 2007), whereas emergent plants directly transport CH4
to the atmosphere, resulting in greater CH4 emissions (Bastviken et al.,
2004). In addition, a high abundance of submerged plants markedly re-
duces the ebullition flux of CH4; however, an explanation of these
effects requires further study (Davidson et al., 2018). The loss of macro-
phytes on eutrophic freshwater affects GHG fluxes, considering the cov-
erage and abundance of macrophytes and that submerged plants
effectively decrease CH4 efflux.
GHG emissions from eutrophic freshwaters are further affected if
algae ultimately become the dominant primary producer. Given their
higher CO2 uptake rate as well as CO2 consumption efficiency compared
with aquatic macrophytes (Tsai et al., 2017), algae play an important
role in CO2 bio-fixation via specific carbon-concentrating mechanisms
(Ghosh and Kiran, 2017). Thus, it is reasonable to state that a high abun-
dance of algae in freshwaters effectively reduces CO2 emissions. How-
ever, algae also produce CH4, which is the second-most important
GHG in the atmosphere. CH4 is generally produced under anoxic condi-
tions, but cyanobacteria readily produce CH4 even in the oxic zone by
converting fixed inorganic carbon and subsequently release this potent
GHG under both light and dark conditions (Bižić et al., 2020). Neverthe-
less, the possible biochemical pathways of cyanobacteria in CH4 forma-
tion should be investigated.
In addition, algae also cause high flux of N2O in freshwaters. It has
been estimated that N2O emitted by microalgae merely in eutrophic
lakes equals 18% of the current global N2O fluxes from all rivers, estuar-
ies, and coastal zones (Plouviez et al., 2019). Studies have shown that
green algae produce N2O by converting nitric oxide (NO) via photosyn-
thesis, which is attributed to the flavodiiron proteins and cytochrome
p450 in algal cells (Burlacot et al., 2020). Although algae can produce
N2O, their quantitative effects on N2O production have rarely been in-
vestigated, making it difficult to assess the algal contribution to the
global N2O budget.
4.2. Facilitation of harmful algal blooms
HABs, which are a vital issue in freshwater and marine ecosystems
(Ai et al., 2019), refer to the rapid proliferation and/or high biomass ac-
cumulation of microalgae in the water column, impairing the health of

6
Y. Li, J. Shang, C. Zhang et al.
other aquatic life (Anderson et al., 2012). Eutrophication induced by ex-
cess nutrient inputs degrades water quality leading to the development
and persistence of HABs (Heisler et al., 2008). In addition, the composi-
tion of the nutrient pool in eutrophic freshwaters can also affect HABs
because algae differ in their nutrient preferences (Granéli et al., 2008;
Heisler et al., 2008). Consequently, nutrient imbalances in eutrophic
freshwater cause specific algal species, such as harmful species, to gain
greater competitive advantage over others, promoting the development
of HABs.
HABs are a common consequence of freshwater eutrophication and
an important facilitator of GHG emissions from freshwaters. Field and
laboratory experiments have shown that high GHG fluxes occur during
HABs (Harrison and Matson, 2003; Huang et al., 2019; Yan et al., 2017).
These relationships can be explained by the effects of three factors,
namely algal-derived organic carbon, anoxic conditions, and the ability
of the algae to produce GHGs (Fig. 3). Briefly, labile algal substrates meet
the demands of microbial stoichiometry resulting in the co-
decomposition of different organic matter in the sediments, conse-
quently increasing CO2 and CH4 emissions (Ma et al., 2020). Dense
scums resulting from the development of HABs prevent reoxygenation
of the water; thus, promoting hypoxia and anoxia below the surface of
the blooms (Xing et al., 2011; Yan et al., 2019). These blooms create an-
oxic conditions that promote methanogenesis, as mentioned previ-
ously. Furthermore, the accumulation of algal biomass caused by HABs
are projected to increase fluxes of CH4 and N2O due to the ability of
algae to produce or convert them (Bižić et al., 2020; Burlacot et al.,
2020; Plouviez et al., 2019). Despite increased CH4 and N2O emissions
facilitated by HABs, there is uncertainty about the net effect of HABs
on CO2 emissions due to the imbalance between CO2 consumption by
algal cells and CO2 production by algal decomposition.
Interestingly, HABs induced by freshwater eutrophication can in
turn boost freshwater eutrophication; thus, further affecting GHG emis-
sions (Fig. 3). P mobility and release is markedly stimulated during
HABs, and scientific concern of this phenomenon has increased rapidly.
To date, three major factors have been identified to explain this phe-
nomenon. First, DO concentrations are extremely low at the sediment-
water interface during a HAB, which creates extremely anaerobic and
reducing condition for the dissolution of Fe(III) oxyhydroxides, conse-
quently promoting the release of Fe-bound P from sediments into the
freshwaters (Pearce et al., 2013; Smith et al., 2011). Second, elevated
pH from algal photosynthesis during the development of HABs pro-
motes the release of Fe-bound P because of the breaking of surficial
Fe\\P bonds via competition with OH− (Gao et al., 2012; Xie et al.,
2003). Third, algal decomposition results in the direct release of consid-
erable nutrients from algal cells and the indirect release of P from sedi-
ments (Chen et al., 2016; Zhao et al., 2019). Release of dissolved sulfides
(ΣS2−) from cells helps P release from sediments (Zhao et al., 2019). On
the one hand, solid iron sulfide forms from the combination of ΣS2− and
Fe(II) (Chen et al., 2016; Sulu-Gambari et al., 2016). On the other hand,
Fe(III) oxyhydroxides are chemically reduced by ΣS2− and stored as
acid volatile sulfides (Lehtoranta et al., 2009; Zhao et al., 2019). As a re-
sult, Fe cycling is blocked, leading to the reduction and dissolution of Fe
(III) oxyhydroxide and the promotion of P desorption and release. The
large release of nutrients into freshwaters enhances the eutrophic status
of the water bodies and facilitates the growth of HABs; thus, indirectly
affecting GHG emissions.
5. Feedback loops between freshwater eutrophication and
greenhouse gas emissions
On the contrary, GHG emissions can affect freshwater eutrophica-
tion as mediated by climate change. Under the background of climate
change, average air temperature and the frequency of extreme weather
are increasing and these increases have been particularly marked since
the 1970s (IPCC, 2013). Notably, both climate warming and an increase
in the frequency of extreme weather events can affect freshwater
7
Science of the Total Environment 768 (2021) 144582
eutrophication. Rising global mean temperature under the background
of climate warming has been confirmed to stimulate the release of nu-
trients from sediments via mineralization, consequently boosting the
eutrophic state of freshwaters (Greaver et al., 2016). In addition to tem-
perature, precipitation events are also affected by climate warming, in-
cluding increased rainfall at higher latitudes/part tropics and reduced
rainfall in arid zones (IPCC, 2013). Increased rainfall can further increase
runoff, leading to higher nutrient inputs from land into water bodies,
while reduced rainfall extends hydraulic residence time; thus, increas-
ing nutrient concentrations in water bodies by enhancing evapotranspi-
ration (Jeppesen et al., 2009; Jeppesen et al., 2010). These changes in
precipitation events ultimately stimulate freshwater eutrophication.
Importantly, extreme weather exacerbates the effects of climate
warming on precipitation events, such as increasing the frequency and
magnitude of heavy precipitation, subsequently promoting the washout
of nutrients from land into freshwaters and thus boosting eutrophica-
tion (Greaver et al., 2016; Jeppesen et al., 2009). Given that freshwater
eutrophication promotes GHG emissions, it is proposed that bidirec-
tional feedbacks might exist between freshwater eutrophication and
GHG emissions.
A positive feedback loop has been previously suggested between
GHG emissions and environmental effects (Niinemets et al., 2017).
Freshwater eutrophication is a vital environmental effect, and its feed-
back on GHG emissions has aroused increased scientific concern. Fig. 4
shows the positive feedback loops between freshwater eutrophication
and GHG emissions. Among the positive feedback loops, freshwater eu-
trophication and GHG emissions are strengthened by each other; there-
fore, increasing the cost but reducing the effectiveness of mitigation of
both freshwater eutrophication and GHG emissions (Halpern et al.,
2007; Su et al., 2019). Considering the difficulties in the conservation
of freshwater ecosystems and the Earth's climate, it is important to
identify the strength of positive feedback loops between freshwater eu-
trophication and GHG emissions.
It has been well known that freshwater eutrophication and climate
change are two major worldwide threats, and these two threats will
co-occur and get strengthened in the future, causing more serious dam-
age to the climate and ecosystems on a global scale. The function and re-
silience of natural ecosystems are affected by positive feedback loops,
which impede the efficacy of mitigation measures for both freshwater
eutrophication and GHG emissions (Su et al., 2019). Freshwater eutro-
phication is predicted to promote GHG emissions by affecting abiotic
and biotic factors; therefore, making climate change more severe. At
the same time, climate change is expected to exacerbate symptoms of
eutrophication, such as increasing the nutrient concentrations in fresh-
waters and negatively affecting the cover and abundance of submerged
plants (Feuchtmayr et al., 2009; Kosten et al., 2009; Moss, 2011). In ad-
dition, rising temperatures because of climate change are expected to
promote the development and persistence of worldwide phytoplankton
blooms (Ho et al., 2019; Paerl and Paul, 2012). The occurrence of either
freshwater eutrophication or climate change will exacerbate the other
threat, calling for studies to assess the possible effects of the combina-
tion of both.
Interestingly, the impacts of climate change and freshwater eutro-
phication or merely climate change on GHG emissions are complex for
three main reasons. First, there is a synergy between warming and eu-
trophication in enhancing CH4 emissions (Davidson et al., 2018). This
observation can be explained by the higher temperature sensitivity of
methanogenesis relative to methanotrophy triggered by eutrophication
(Sepulveda-Jauregui et al., 2018) and the great CH4 ebullition flux in-
duced by the low abundance of aquatic macrophytes in eutrophic
freshwaters (Davidson et al., 2018). Second, the proliferation of phyto-
plankton, which is promoted by climate warming and freshwater eutro-
phication, not only releases GHGs but also anti-GHGs, such as dimethyl
sulfide (DMS) and dimethyl disulfide (Deng et al., 2020). DMS, mainly
emitted by algae, strongly reduces solar radiation and partially offsets
the effects of GHG emissions (Malin and Kirst, 1997). Third, climate
Y. Li, J. Shang, C. Zhang et al. Science of the Total Environment 768 (2021) 144582

Fig. 4. Conceptual diagram of the feedback loops between freshwater eutrophication and greenhouse gas (GHG) emissions. Promoted GHG emissions can alter the Earth's climate and thus
stimulate freshwater eutrophication by increasing the nutrient loadings (indicated by solid arrows). In addition, symptoms of freshwater eutrophication, such as dominant primary
producer and harmful algal blooms (HABs), can also be affected (indicated by dashed arrows). The responses of freshwater eutrophication to the promoted GHG emissions (indicated
by solid arrows) lie not only in generating abiotic conditions that favor the production and emissions of greenhouse gases (GHGs) but also in mediating biotic processes that stimulate
GHG emissions.

warming has already led to increased freshwater acidification and strati-
fication (Carey et al., 2012; Griffith and Gobler, 2020), and these changes
will further affect GHG emissions. Deposition of acid nitrogen/sulfur com-
pounds and rising atmospheric levels of CO2 have caused widespread
acidification in many freshwater ecosystems (Greaver et al., 2016; Paerl
and Paul, 2012), which promotes N2O emissions due to the facilitation
of aquatic ammonia-oxidizing microorganisms (Frame et al., 2017).
Warming strengthens the magnitude and duration of stratification; there-
fore, limiting CH4 diffusion across the thermocline and enhancing CH4
storage (West et al., 2016). Owing to the complex relationship among
GHG emissions, climate change, and freshwater eutrophication, it is nec-
essary to quantify the strength of the positive feedback loops between
freshwater eutrophication and GHG emissions and test the net effects of
freshwater eutrophication and climate change on overall GHG emissions.
6. Conclusions and perspectives
Recently, low oxygen content, abundant organic matter and nutri-
ents, dominant primary producers and HABs in eutrophic freshwaters
have been found to favor GHG production and emissions. Increased
freshwater eutrophication projected in the future is likely to significantly
promote aquatic GHG fluxes and strengthen the greenhouse effect;
therefore, resulting in serious environmental problems and socioeco-
nomic loss. Management agencies must implement measures to alleviate
freshwater eutrophication, which will not only improve water quality
but also reduce GHG emissions. Attempts to reduce nutrient inputs, bal-
ance nutrient stoichiometry, and maintain a clear, macrophyte-
dominated water regime are indispensable. In addition, a deeper and
more detailed understanding on the future dynamics of freshwater eu-
trophication and GHG emissions is necessary for management agencies
to implement effective mitigation measures and protect freshwater eco-
systems and the Earth's climate. This should begin by quantifying the ef-
fects of key influencing factors or indicators, which is a major
undertaking and requires close cooperation between freshwater ecolo-
gists, meteorologists, modelers, and management agencies.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgement
This study was supported by the National Key R&D Program of China
(2019YFC0408301), the National Natural Science Foundation of China
(51779076); the Fundamental Research Funds for the Central
Universities (B210202101); the Foundation for Innovative Research
Groups of the National Natural Science Foundation of China
(51421006); the Funds for Key Research and Development Project of
Science and Technology Department of Jiangsu Province (BE2018738);
the Six Talent Peaks Project in Jiangsu Province (2016-JNHB-007); the
333 Talent Project Foundation of Jiangsu Province and the Priority
Academic Program Development of Jiangsu Higher Education Institutions
(PAPD).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2020.144582.

8
Y. Li, J. Shang, C. Zhang et al.
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