Bubbles adsorb and transport particulate matter in a variety of
natural and engineered settings, including industrial, freshwater, and
marine systems. While methane-containing bubbles emitted from anoxic
sediments are found widely in freshwater ecosystems, relatively little
attention has been paid to the possibility that these bubbles transport
particle-associated chemical or biological material from sediments to
surface waters of freshwater lakes. We triggered ebullition and quantified
transport of particulate material from sediments to the surface by bubbles
in Upper Mystic Lake, MA, and in a 15 m tall experimental column. Particle
transport was positively correlated with the volume of gas bubbles released
from the sediment, and particles transported by bubbles appear to originate
almost entirely in the sediment, rather than being scavenged from the water
column. Concentrations of arsenic, chromium, lead, and cyanobacterial cells
in bubble-transported particulate material were similar to those of bulk
sediment, and particles were transported from depths exceeding 15 m,
implying the potential for daily average fluxes as large as 0.18
Deterioration of water quality is widespread and expected to become more
acute with increased urbanization and climate change (Zhang, 2016; Paerl
et al., 2011). In a 2012 national assessment, 15.2 % of surveyed lakes in
the US were categorized as “most disturbed” due to the concentration of
cyanobacteria, a significant increase in lakes with this categorization
(8.3 %, 95 % confidence intervals 4.0 %–12.5 %) over the 2007 assessment
(U.S. Environmental Protection Agency, 2016). A concentration
of 10
Because sediments are typically major repositories of contaminants
(Nriagu et al., 1996; Pan and Wang, 2012; Taylor and Owens, 2009), it is
important to understand the processes leading to contaminant mobilization.
Metals can be mobilized from sediments via solubilization by
oxidation-reduction reactions, as well as by sediment resuspension, acidification,
or bioturbation (Calmano et al., 1993; Eggleton and Thomas, 2004;
Schaller, 2014; Schindler et al., 1980). Likewise, overwintering
cyanobacteria and algae concentrated in the sediments are mobilized through
germination, wind-induced resuspension, or bioturbation (Ramm et al.,
2017; Verspagen et al., 2004; Stahl-Delbanco and Hansson, 2002). In some
cases, the number of resting cells in sediment can be predictive of the
severity of subsequent bloom events (Anderson et al., 2005). Previous
research showed that recruitment from sediments of the potentially toxic
cyanobacterium
An alternative mechanism for vertical transport of metals and cells from sediment to surface water could be bubble-facilitated transport. Bubbling from anoxic sediments, driven by methanogenesis, is widespread in freshwater systems (Bastviken et al., 2011; Deemer et al., 2016), and bubbles are known to be effective particle transporters. Bubble particle flotation, a process by which amphiphilic particles attach to a bubble's gas–water interface and are transported upwards during bubble rise, is used extensively in industry for applications such as separating valuable minerals from gangue (Min et al., 2008; Rodrigues and Rubio, 2007), removing ink during paper recycling (Vashisth et al., 2011), recovering desirable proteins and microorganisms from industrial bioreactors (Schugerl, 2000), and treating wastewaters (Aldrich and Feng, 2000; Lin and Lo, 1996; Rubio et al., 2002). Bubble-mediated particle transport also occurs in the open ocean where bubbles are injected into the water by breaking waves, scavenge surface-active particles as they rise, and then deposit these particles on the ocean surface (Aller et al., 2005; Blanchard, 1975; Wallace et al., 1972; Liss, 1975).
Despite this previous work, little is known about the importance of particle transport by bubbles in freshwater systems. Bubbles produced by methanogenesis in anoxic sediments are prevalent in freshwater systems, and bubbles are released to the surface during drops in hydrostatic pressure, sediment disturbance, or upon sufficient gas accumulation (Chanton et al., 1989; Joyce and Jewell, 2003; Scandella et al., 2011; Liu et al., 2016; Maeck et al., 2014; Varadharajan and Hemond, 2012). Bubble flotation could thus potentially provide a chemical and biological link from deep water to surface waters that would otherwise not occur through advective or eddy-diffusive transport alone. Additionally, the relatively rapid rise time of bubbles limits the time available for oxidation reactions and suggests that particulate matter from the hypolimnion could reach the lake surface in a reduced state, with possible consequences for both toxicity and reactivity. Some evidence does suggest that bubbles can transport polycyclic aromatic hydrocarbons (Viana et al., 2012) and manufactured gas plant tar from sediments (McLinn and Stolzenburg, 2009). Additional work has shown that bubble-mediated transport of microorganisms including methane-oxidizing bacteria (MOB) is an important mechanism connecting benthic and pelagic populations at 10 m water depth (Schmale et al., 2015). However, researchers in the previous study were unable to quantify the importance of bubble-mediated transport to overall recruitment of pelagic MOB populations, and the extent of bubble particle flotation in aquatic systems remains unknown.
The present study is motivated by authors' observations of particle accumulations associated with bubbling events at Upper Mystic Lake (UML), where bursting bubbles often left black particles distributed on the water surface in a ring pattern (Fig. S1 in the Supplement). Particles were also observed at the air–water interface in bubble traps during long-term deployments (data not shown). The significant volume of gas observed to bubble from UML during previous studies (Delwiche and Hemond, 2017; Varadharajan and Hemond, 2012), together with strong thermal stratification suppressing other mechanisms of sediment transport to the surface, led to the hypothesis that bubbles could serve as a relatively important mode of particle transport from the sediment to the water surface. This potential transport pathway could be relatively more important for metal and cyanobacteria transport in eutrophic, deep, stratified lakes, such as UML.
In the present study, we quantified particle transport by bubbles in UML, an
urban lake with a history of sediment contamination. We also used a 15 m
tall bubble column to study bubble-mediated particle transport under
controlled lab conditions. Given the expected importance of bubble size on
key characteristics (e.g., surface area, buoyancy, diffusion of gas), we used
a bubble size sensor (Delwiche et al., 2015; Delwiche and Hemond, 2017)
to measure bubble diameter distribution both in the lake and in the
laboratory. We address the following questions:
How much sediment is transported to the surface through ebullition? How does bubble-mediated sediment transport contribute to metal cycling? How does bubble-mediated sediment transport contribute to cyanobacteria
recruitment to the upper water column?
UML in Arlington, MA, is an urban, dimictic kettle lake with an average depth
of 15 m, a maximum depth of 24 m, and a surface area of 0.58 km
Years of field observations at UML have provided a thorough picture of the
typical hydrological conditions in the lake. Significant volumes of gas are
produced from the sediments, which escape to the surface via ebullition,
resulting in an average release rate of 22 mL bubble volume m
Bubble-transported particles were collected from both the laboratory column
and the lake in 350 mL plastic sampling cups affixed either to the top of a
custom bubble size sensor (sensor described previously; Delwiche et al.,
2015; Delwiche and Hemond, 2017) or to the top of a collection funnel (the
bubble sensor was used in 2017 sampling; the funnel alone was used for
sampling in 2018). The plastic sampling cup lid contained a barbed bulkhead
fitting connected via flexible plastic tubing to an on–off valve and a
quick-release adapter (Fig. S2). The sampling cup, valve, and adapter were
connected to the custom bubble size sensor or collection funnel with
flexible tubing. All bubbles rising through the bubble size sensor or
collection funnel entered the flexible tubing and rose into the sample cup.
The interaction of bubbles with the flexible tubing resulted in visible
particle attachment to the tubing, making our estimates of particle mass
transport a lower bound. The sample cup lid contained a secondary valve to
release water upon bubble entry. All sample cups were soaked in 5 %–10 %
reagent grade
On 17 October 2017 we sampled for bubble-mediated sediment mass fluxes and
associated particulate metal fluxes in an area of the lake previously found
to have relatively high ebullition rates (42.432 latitude,
After bubble triggering, the bubble size sensor was positioned above the
bubble plume and 1 m below the water surface. Bubbles exiting the sensor,
together with any particles adhered to the bubble–water interface, were
collected in the sample cup described previously. Several anchor drops
within an area of approximately 10 m by 10 m were required to intercept a
sufficient number of bubbles for mass quantification per sample, and we
intentionally collected samples with different total gas volumes. We
collected blank water samples to correct for background contributions of
particulate matter, arsenic, lead, and chromium. Bubbling resulted in the
visual accumulation of particles at the surface (Fig. S1) and in the
sampling cup. During a separate field visit in November 2017 we used an
Ekman dredge to collect sediment and stored the sediment in a 5 gal (18.9 L)
bucket below 4
On 26 June 2018 we sampled for cyanobacteria bubble transport using similar
procedures, except we used a simple inverted funnel instead of a custom
bubble size sensor to intercept rising bubbles. The sampling funnel was
placed 10 m below the water surface, where cyanobacteria concentrations were
expected to be lower than the surface based on previous observations
(Preheim et al., 2016) to reduce sample contamination with
cyanobacteria from the surrounding water column. Water temperature
measurements taken using a Hydrolab sonde (Hach Co.) confirmed that the
thermocline depth was above 10 m in this location during sampling (Fig. S3).
We collected 30–40 mL of water samples at 15, 11, 10, and 1 m depths for
background cell concentration counts and gathered sediment grab samples
with an Ekman dredge. All sample cups were sterilized prior to use by
rinsing with 10 % bleach followed by 70 % ethanol and deionized, sterile
water, and cups were filled with sterile water prior to sample collection.
Samples were stored in a dark cooler on ice and were refrigerated upon
return to the lab. On 26 June 2018 we also used an Ekman dredge to collect a
bulk sediment sample, which was kept in a dark refrigerator at 4
To study bubble particle shedding and scavenging, we built a 15 m tall
bubble column in the laboratory stairwell. The column is composed of four
sections of 6 in. (15.3 cm) nominal diameter transparent polyvinyl chloride
(PVC) pipe joined by threaded unions with O-ring seals. The base of the
column is a reducing tee fitting with a removable spigot for drainage, and
the column was filled from the top with tap water. We built a sediment
container connected to
We conducted one set of column experiments in February 2018 to quantify
shedding, scavenging, and metal transport and another set of column
experiments in February 2019 to quantify cyanobacterial transport. For the
shedding and metal transport experimental runs, we filled the sediment bed
with sediment collected from the same site as ebullition experiments during
our November 2017 field visit, and we injected 50 mL of air at 0.7 mL min
We filtered the field samples collected from UML for metals analysis within
24 h of sampling with preweighed Whatman grade 41 quantitative cotton
filters (nominal pore size 20
We filtered bubble column samples using preweighed 5.0 and 0.2
For both the field and bubble column cyanobacterial transport experiments,
we filtered a subset of the samples within 24 h with 0.2
For quantitative polymerase chain reaction (qPCR) analysis on the June 2018 bulk sediment samples, 0.13 g of wet sediment was suspended in 15 mL of sterile water and then filtered as described above. For microscopy cell counts, 0.14 g wet sediment was preserved in 2 % by volume paraformaldehyde. Water column samples from the June 2018 field campaign were also preserved in 2 % by volume paraformaldehyde for cell counts. For qPCR analysis of the June 2018 sediment samples before use in the bubble column, we filtered 0.7 g of wet sediment (0.007 g dry sediment). For microscopy cell counts of the June 2018 sediment samples before use in the experimental bubble columns, we placed 0.8 and 2.0 mg of wet sediment (0.08 and 0.18 mg dry weight, respectively) into 10 mL of 10 % formalin.
Cyanobacteria cell counts were assessed through quantitative polymerase
chain reaction and microscopy. These two methods estimate
cyanobacteria cell numbers by targeting different features of
cyanobacterial cells. qPCR targets the unique genetic signatures in the 16S
ribosomal RNA (rRNA) gene of cyanobacteria (Nubel et al., 1997) to
estimate cell number from gene copy numbers. Microscopy takes advantage of
the unique fluorescence spectra of cyanobacterial photosynthetic pigments to
identify cells (Salonen et al., 1999). Positive control
To estimate the total number of cells in the
For cyanobacteria cell quantification with (qPCR), DNA was extracted using
PowerWater kits (Qiagen, Inc) following the manufacturer's protocol, with
the addition of 20
The contribution (%) of ebullition to cyanobacteria recruitment
(
Both field and bubble column experiments demonstrate that bubbles can
transport particles from the sediment to the lake surface. A positive
correlation (
Total particle mass in milligrams (mg) associated with the bubbles captured during each field campaign with bubble-triggering events in October 2017 (filled circles) and June 2018 (open circles). Triggering events yielded different bubble volumes (given in mL).
These particle loadings on bubbles, and any ecosystem-wide flux estimates derived from them, must be qualified by the fact that neither triggered bubbles nor bubbles in the bubble column fully replicate natural bubbling. In particular, the triggering of bubbles with an anchor may have raised plumes of suspended sediment through which some fraction of produced bubbles had to rise, and within which the possibility of scavenging should be considered. Likewise, bubbles could shed particles partway up the water column during rise. To estimate the significance of particle shedding, we used the bubble column to compare transport rates from bubbles released at 5, 10, and 15 m depths (Fig. 2). We found no significant difference in transport rates from any depths, suggesting that net particle shedding was not a major process. We did however note that the first bubble column test conducted after repositioning the sediment source yielded a higher particle transport rate than those found in subsequent tests (Fig. 2), consistent with the intuitively reasonable possibility that mechanical sediment disturbance can affect particle loading on bubbles. We also note that while bubbles do dissolve as they rise, bubbles in the size range seen during this study remain relatively constant in volume during their rise through 15 m of water column because dissolution is partially compensated for by bubble expansion during rise (Delwiche and Hemond, 2017), and we therefore do not expect bubble dissolution to substantively impact particle shedding.
Transported particle mass per liter of gas bubbled in the large bubble column, as a function of bubble release depth. Solid circles represent samples where bubbles were emitted from the sediment bed; diamonds represent samples where gas was bubbled directly above the sediment bed. Hollow circles around solid circles denote samples with recently disturbed sediments.
To observe the possible extent of bubble scavenging of particles from the water column, we compared data from 5 and 10 m column experiments to samples gathered when gas was bubbled from several centimeters above sediment, thus allowing maximum opportunity for scavenging to occur. We conducted the scavenging tests when the water column was visibly turbid and contained a plume of suspended particles from previous tests. Particle mass scavenging represented only around 10 % of the mean particle loading for bubbles in the 5 and 10 m experiments (gray diamonds in Fig. 2), indicating that while scavenging rates were nonzero, the large majority of the particulate matter transported to the top of the water column originated in the sediment. Taken together, the minimal particle shedding and particle scavenging in column experiments suggests that particles observed on bubbles in the field, even when bubble release was triggered, mainly originated in the sediment.
While bubbles transported sediment directly from the bottom of the laboratory column to the water surface, a vertical distance of 15 m, there appears to be no reason that transport of particles from significantly larger depths cannot occur. Such transport provides a direct chemical and biological link between sediment and surface waters, and this could be the dominant link between deep sediments and the surface water during months of stratification. However, many questions remain regarding bubble-mediated transport in natural systems, including how the change in water density at the thermocline affects bubble rise and associated chemical and biological material.
Bubble volume has been found to significantly affect particle flotation rates in industrial processes (Yoon and Luttrell, 1989), and therefore it is important to compare the anchor-triggered bubble sizes to naturally occurring bubble sizes to understand how our measured transport rates may reflect naturally occurring transport rates. Anchor-triggered bubbles were significantly smaller (average diameter 5.6 mm) than those measured for natural bubbling events (average diameter 6.4 mm) during a 2016 field campaign (Fig. S7; Delwiche and Hemond, 2017), even though relatively high bubble flux events (such as those triggered by anchor dropping) can lead to some bubble coalescence within the funnel constriction in the bubble size sensor (as described previously; Delwiche and Hemond, 2017).
However, both natural and triggered bubbles were still very large compared to bubbles used in traditional flotation chambers (Yoon and Luttrell, 1989; Rubio et al., 2002). While research on particle flotation for large bubbles is limited, several previous studies have found that differences in particle transport rates decrease for bubbles above 1 mm diameter (Dai et al., 1998; Koh and Schwarz, 2008), indicating that particle transport rates should be similar between natural and triggered bubbles. Bubble sizes measured in the cyanobacteria transport experiment displayed a bimodal distribution (Fig. S8) that was not observed in other bubble experiments. This bimodal distribution could be a result of artificially pumping gas into the sediment, but the impact of this on particle transport is unknown.
The data on bubble particle mass transport clearly shows that bubbles are
capable of transporting particles from relatively deep depths, and minimal
rates of particle shedding and scavenging in the water column suggest that
these particles originate primarily in the sediment. Concentrations of
arsenic, chromium, and lead in the bubble-transported particulate matter
collected during field experiments were similar to concentrations in the
sediment (Fig. 3). Bubble-transported particles contain arsenic, chromium,
and lead at average ratios of 100, 120, and 240
Comparison between mass of arsenic, chromium, and lead per kilogram of sediment (open triangles) and bubble-transported particulate matter (solid circles). The standard deviation scale is similar to point size and therefore omitted for figure clarity.
In addition to the heavy metal results indicating that the transported
particles are from the sediment, biological evidence also suggests a
sedimentary origin. All particle samples transported by bubbles contained an
abundance of biological structures (Fig. S10), such as the apparent head
shields and carapaces of
The presence of arsenic and other heavy metals in the bubble-transported
particles could have significant implications for chemical cycling in
aquatic ecosystems. Measured rates of arsenic flotation in field samples
were about
Chemical amounts observed in bubble traps associated with
bubble-mediated transport of sediment particles.
The concentration of cyanobacteria cells (as measured by quantitative PCR) increases in the experimental water column and bubble traps after initiating bubbling within sediments. The background concentration of cyanobacteria cells in the water column was initially low (“Before bubbling”) but increased after bubbling air through the sediment. The concentration of cells in the bubble trap increased even if bubbles did not pass directly through sediment but instead originated above the sediment bed (“Bubbling above sediment”) from cells contaminating the surrounding water column. However, the highest concentration of cyanobacteria in the bubble trap was observed when initiating bubbling from within the sediment (“Bubbling within sediment”) from direct transport of cells from the sediment into the bubble trap. The increase in cell concentration in both the water column and the bubble trap after bubbling within sediment is evidence for cyanobacteria transport via bubble floatation. Error bars show standard deviation across measurements.
This estimate of daily arsenic flux can be compared with historical
measurements showing significant arsenic accumulation within the epilimnion
at rates exceeding 30
Although bubble-facilitated transport does not appear to dominate arsenic
transport in UML, much higher ebullition rates have been reported elsewhere
in the world (Deemer et al., 2016). For example, a midlatitude reservoir
in Switzerland was reported to have an order of magnitude higher ebullition
flux (0.225 L m
Since cyanobacteria are known to overwinter in lake sediments,
bubble-mediated transport could be one mechanism by which resting cells
inoculate the upper water column. Bubble column experiments showed that
bubble-transported particulate matter contained cells at approximately 30 cells mL
To assess the likelihood that bubble-mediated cell transport could
significantly inoculate surface waters, we use the upper transport estimate
of
Given the potential impact on bloom formation, we compared this source of
cells to other pathways of cell recruitment to the lake surface, especially
in deep, stratified lakes like UML. Cyanobacteria are thought to largely be
recruited to surface waters from shallow areas due to a combination of
higher light, temperature, and oxygen levels that promote germination, as well as increased wind-driven sediment resuspension (Ramm et al., 2017). While
sediment cyanobacteria concentrations are higher in deeper areas of the
lake, cells are not able to germinate because of the dark, anoxic conditions
in deep, eutrophic lakes (Ramm et al., 2017). Bubble-mediated transport
is a mechanism by which this large reservoir of “lost” cells in deep
sediments could contribute to overall recruitment to the surface waters. To
determine the potential contribution of bubble-mediated transport to
cyanobacteria recruitment to the surface, we assume that germination does
not occur significantly past the oxycline (12 m) in UML between June and
October, as low oxygen concentrations and low light levels prevent germination,
and wind-driven mixing cannot resuspend sediments across the shallow
thermocline (Varadharajan, 2009). We also assume that cells
resuspended in the spring overturn in March would have germinated, settled,
lysed or have been consumed by grazers by June (e.g., Tijdens et al.,
2008; Verspagen et al., 2005). Furthermore, we do not include external
inputs of cyanobacteria to the lake, such as from the river (e.g.,
Bouma-Gregson et al., 2019) or air (Seifried et al., 2015;
Lewandowska et al., 2017; Evans et al., 2019). Since literature estimates of
recruitment rates for these sources are lacking, we assume these inputs are
small compared to shallow sediment and bubble-mediated recruitment. Using
the maximum observed recruitment rate of
Bubble particle transport between the sediment and surface of UML is a novel transport pathway capable of moving particulate matter upwards through a stratified water column, over depths of 15 m or greater, without shedding a major fraction of their particle burden or accumulating large amounts of additional particles as they rise. Bubble-facilitated metal transport in present-day UML appears minor compared to surface inflows, but lakes with higher ebullition flux or more contaminated surficial sediments may experience more significant chemical transport from contaminated sediments. Bubble-mediated transport of cyanobacteria cells may contribute substantially to cellular recruitment from the sediment, but the uncertainties in our measurements make these estimates speculative. Bubble transport is expected to be particularly important in deep, eutrophic lakes in which alternative mechanisms of sediment regeneration to surface waters are limited. Further work is warranted to more thoroughly quantify this ebullitive transport pathway and its implications for chemical and biological cycling. In addition, future work should include alternative methods of bubble triggering as well as the quantification of particle transport rates on naturally occurring bubbles.
All data necessary to validate the research findings are available on JHU
Dataverse,
The supplement related to this article is available online at:
KD, HH and SPP designed the experiments and KD and JG carried out experimental work. KD, JG and SPP analyzed the data. KD prepared the manuscript with contributions from all coauthors.
The authors declare that they have no conflict of interest.
Resources for this work were provided by the Singapore-MIT Alliance for Research and Technology, the MIT Center for Environmental Health Science, MIT Superfund Research Program, the MIT Martin Family Fellowship to Kyle Delwiche, and the W. E. Leonhard 1941 professorship to Harold Hemond.
This research has been supported by the National Science Foundation, Division of Earth Sciences (grant no. EAR-1045193), and the National Institutes of Health, National Institute of Environmental Health Sciences (grant no. P42 ES027707 and P30-ES002109).
This paper was edited by Manmohan Sarin and reviewed by Dileep Kumar and three anonymous referees.