Abigail S. L. Lewis1, Madeline E.
Schreiber2, B. R. Niederlehner1,
Arpita Das1, Nicholas W. Hammond2,
Mary E. Lofton1, Heather L. Wander1,
Cayelan C. Carey1
1Department of Biological Sciences, Virginia Tech,
Blacksburg, Virginia, USA
2Department of Geosciences, Virginia Tech, Blacksburg,
Virginia, USA
Corresponding author: Abigail S. L. Lewis (aslewis@vt.edu)
Key Points:
- Short-term (2–3 week) periods of hypoxia decreased iron-bound organic
carbon and total organic carbon in reservoir sediments
- Multiannual periods of hypoxia increased total organic carbon in
sediment, likely through decreased rates of respiration
- A substantial fraction of sediment organic carbon
(~30%) was bound to iron in these two freshwater
reservoirs
Abstract
Freshwater lakes and reservoirs play a disproportionate role in the
global carbon budget, sequestering more organic carbon (OC) than ocean
sediments each year. However, it remains unknown how global declines in
bottom-water oxygen concentrations may impact OC sequestration in
freshwater sediments. In particular, associations between OC and iron
(Fe) are hypothesized to play a critical role in stabilizing OC in
sediment, and these complexes can be sensitive to changes in oxygen.
Under low-oxygen (hypoxic) conditions, Fe-bound OC (Fe-OC) complexes may
dissociate, decreasing OC sequestration. However, rates of OC
respiration are also lower under hypoxic conditions, which could
increase OC sequestration. To determine the net effects of hypoxia on OC
and Fe cycling over multiple timescales, we paired whole-ecosystem
experiments with sediment incubations in two eutrophic reservoirs. Our
experiments demonstrated that short (2–4 week) periods of hypoxia can
increase Fe and OC concentrations in the water column while decreasing
OC and Fe-OC in sediment by 30%. However, exposure to seasonal hypoxia
over multiple years was associated with a 57% increase in sediment OC
and no change in Fe-OC. These results indicate that the large sediment
Fe-OC pool (~30% of sediment OC) contains both
oxygen-sensitive and oxygen-insensitive fractions, and over multiannual
timescales, OC respiration rates play a greater role than Fe-OC
protection in determining the effect of hypoxia on sediment OC content.
Consequently, we anticipate that global declines in oxygen
concentrations will alter OC and Fe cycling, with the direction and
magnitude of effects depending upon the duration of hypoxia.
Plain Language Summary
Freshwater lakes and reservoirs (hereafter: lakes) play a remarkably
important role in the global carbon cycle. Every year, more organic
carbon (e.g., leaves, soil) is buried in lake sediments than in the
sediments of all of the world’s oceans. However, these organic carbon
inputs can also be decomposed, releasing greenhouse gases. The extent to
which lakes bury carbon vs. release greenhouse gases may be changing, as
oxygen concentrations are decreasing in the bottom waters of many lakes
around the world. Here, we added oxygen to the bottom waters of a whole
lake to test how changes in oxygen concentration affect carbon cycling.
We found that over short timescales (weeks), low oxygen conditions
decreased the amount of carbon in sediment by breaking apart chemical
complexes with iron that can help retain carbon in sediment. However,
over long timescales (years), low oxygen conditions appeared toincrease carbon burial by decreasing the rate at which carbon
inputs were decomposed. These results suggest that declining oxygen
concentrations in lakes around the world may have important effects on
global carbon cycling, with the direction and magnitude of the impact
depending on the duration of low oxygen conditions.
1. Introduction
Freshwater lakes and reservoirs are increasingly recognized as hotspots
in the global carbon cycle (Bastviken et al., 2011; Battin et al., 2009;
Carey, Hanson, et al., 2022; Raymond et al., 2013; Tranvik et al.,
2018). Due to high organic carbon (OC) loading from the surrounding
watershed, more OC is buried in lakes and reservoirs than in ocean
sediments each year (Dean & Gorham, 1998; Knoll et al., 2013; Mendonça
et al., 2017; Pacheco et al., 2014). Much of this OC remains sequestered
in the sediments, especially in reservoirs, which alone account for 25%
of the global carbon sink from all terrestrial and freshwater sources
(Le Quéré et al., 2015). However, OC inputs can also be respired to
carbon dioxide and methane, making lakes and reservoirs a source of
greenhouse gas emissions equivalent to 20% of the global emissions from
fossil fuels (Deemer et al., 2016; DelSontro et al., 2018). To refine
global carbon budgets and manage water resources in a changing world, it
is important to understand what factors control the balance between OC
sequestration and carbon emissions in these ecosystems.
Recent research suggests that associations between OC and iron (Fe) may
play a critical role in OC sequestration across soils and marine
environments (e.g., Hemingway et al., 2019; Kramer & Chadwick, 2018;
Lalonde et al., 2012), and these associations are hypothesized to also
be important in freshwater sediments (Björnerås et al., 2017; Peter et
al., 2016; von Wachenfeldt et al., 2008; Weyhenmeyer et al., 2014). Fe
can promote OC stability through multiple mechanisms, including
occlusion of OC in aggregates, which can result in physical
inaccessibility to microbial degradation and subsequent burial of OC in
deeper soil or sediment horizons (Kleber et al., 2015 and references
therein). Consequently, protection of OC through complexation with Fe
may facilitate OC sequestration over decades to millennia (Kleber et
al., 2015; Lalonde et al., 2012 and references therein)
Over shorter timescales (days to weeks), Fe-bound OC (Fe-OC) complexes
are sensitive to the redox conditions of the surrounding environment
(Figure 1). Fe-OC complexes form under oxic conditions (Riedel et al.,
2013), as Fe(III) is more effective at complexing with organic matter
than Fe(II) (Nierop et al., 2002). Under hypoxic (reducing) conditions,
OC can be released from Fe-OC complexes through Fe(III) reduction and
dissolution (e.g., Pan et al., 2016; Patzner et al., 2020; Skoog &
Arias-Esquivel, 2009), which can either result directly from hypoxia or
through resultant increases in pH that promote OC release (Kirk, 2004;
Thompson et al., 2006). Given these conflicting patterns—i.e., that
Fe-OC complexes can be preserved over decades to millennia and yet may
be unstable under the reducing conditions which commonly occur on day to
month timescales in aquatic sediments—it remains unclear how changing
oxygen dynamics will affect coupled OC and Fe cycling in freshwater
ecosystems.
Currently, the duration of bottom-water hypoxia (low oxygen conditions)
is increasing in many lakes and reservoirs around the world
(Bartosiewicz et al., 2019; Jane et al., 2021; Jenny et al., 2016;
Williamson et al., 2015), which could have varying consequences for OC
sequestration (Figure 1). In many dimictic lakes and reservoirs,
bottom-water hypoxia is interrupted by oxic conditions during spring
mixing and fall turnover, resulting in dynamic oxygen conditions on the
week to month scale. Combined, these short-term patterns sum to
determine the net role of lakes and reservoirs in the global carbon
cycle over multiannual timescales. Periods of hypoxia have the potential
to decrease OC sequestration through reductive dissolution of Fe(III) in
Fe-OC complexes (Chen et al., 2020; Huang et al., 2021; Patzner et al.,
2020). However, hypoxia also has the potential to increase OC
sequestration by decreasing the rate of OC respiration (Carey et al.,
2018; Carey, Hanson, et al., 2022; Hargrave, 1969; Peter et al., 2017;
Sobek et al., 2009; Walker & Snodgrass, 1986), particularly if Fe-OC
complexes are resistant to, or protected from, changes in oxygen
concentrations in overlying water. Decreased OC respiration rates under
hypoxic conditions is thought to occur primarily because respiration is
less thermodynamically favorable in the absence of oxygen (e.g., Arndt
et al., 2013; LaRowe & Van Cappellen, 2011). Because reductive
dissolution of Fe(III) in Fe-OC complexes and decreased OC respiration
under hypoxic conditions would have divergent effects on total OC
sequestration, understanding the relative importance of these two
processes across multiple timescales is critical for predicting the
effect of hypoxia on OC sequestration in the bottom waters of lakes and
reservoirs (Figure 1).
To date, few studies have explicitly examined Fe-OC in freshwater lakes
and reservoirs, and those that have provide preliminary evidence that
Fe-OC complexation may be lower in freshwater environments compared to
better-characterized marine systems. Peter and Sobek (2018) analyzed
Fe-OC in surficial sediment from five boreal lakes that spanned a
gradient of oxygen conditions and found that less than 11% of sediment
OC was bound to Fe, in comparison with ~20% across a
range of primarily marine sediments (Lalonde et al., 2012). Further,
Peter and Sobek (2018) found no association between Fe-OC content in
sediment and oxygen in overlying water. However, it should be noted that
the lakes in that study were particularly high in dissolved OC (DOC)
concentrations (9–42 mg/L DOC), and may not be representative of all
freshwater ecosystems. Bai et al. (2021) studied Fe-OC along a salinity
gradient in a subtropical tidal wetland and similarly found that
freshwater areas had lower levels of Fe-OC (18% of sediment OC in
freshwater and 29% in saltwater), but these results were attributed
primarily to wetland plant characteristics, which may not be relevant in
the bottom waters of lakes and reservoirs.
Despite limited research on Fe-OC in freshwater sediments, there are
multiple reasons to expect that Fe may play an important role in OC
sequestration in some freshwater ecosystems. Concentrations of Fe and
DOC are strongly correlated in many freshwaters (Björnerås et al., 2017;
von Wachenfeldt et al., 2008; Weyhenmeyer et al., 2014), and aqueous Fe
concentrations are strongly correlated with sediment OC accumulation in
boreal lakes (Einola et al., 2011). Moreover, hypoxic release of DOC
from lake sediments has been well-documented, and is often attributed to
reductive dissolution of Fe (Brothers et al., 2014; Kim & Kim, 2020;
Lau & del Giorgio, 2020; Peter et al., 2017). Still, few studies have
examined whether reactions involving Fe-OC complexes are the driving
force for observed correlations between dissolved Fe and OC (but see
Peter et al. 2018). Furthermore, it remains unknown how the Fe-OC
cycling occurring on sub-annual time scales may affect OC sequestration
on the multi-annual timescales relevant for global carbon budgets.
Analyzing the complex effects of oxygen on coupled OC and Fe cycling
requires multiple experimental approaches. Field surveys have been
effective at identifying correlations between OC and Fe (Björnerås et
al., 2017; von Wachenfeldt et al., 2008; Weyhenmeyer et al., 2014).
However, these observational approaches have limited capacity for
identifying causal relationships. Whole-ecosystem experiments may be
highly effective at identifying real-world impacts of freshwater oxygen
on Fe and OC dynamics, while allowing for important ecosystem-scale
processes such as turbulence and external loading (Carpenter, 1996;
Dzialowski et al., 2014; Schindler, 1998). However, high levels of
variability on a whole-ecosystem scale may limit the detection of subtle
changes in OC and Fe processing. Small-scale incubations may be
particularly useful for identifying changes that result from hypoxia
(i.e., increased DOC and Fe release from sediment, decreased levels of
Fe-OC, changes in sediment OC). However, small-scale incubations are
limited by fouling and changes in microbial communities, among other
microcosm effects, and do not reflect the full suite of processes that
interact to control OC and Fe cycling in lakes and reservoirs.
Consequently, integrating multiple approaches can provide complementary
information on Fe-OC dynamics across spatial and temporal scales and
overcome the limitations of single-approach studies.
To analyze how hypoxia impacts OC and Fe cycling over multiple scales,
this study paired whole-ecosystem oxygen manipulations with laboratory
incubations. We had two objectives: (1) characterize Fe-OC levels in
sediment of two iron-rich reservoirs, and (2) analyze how hypoxia
affects coupled OC and Fe cycling over both short-term (2–4 week) and
multiannual timescales. Through this work, we aimed to provide insight
on how increasing prevalence and duration of hypoxia in lakes and
reservoirs may affect the critical role of these ecosystems in the
global carbon cycle.