- Email: [email protected]
Biological effects on flocculation of fine-grained suspended sediment in natural seawater
Estuarine, Coastal and Shelf Science 228 (2019) 106395
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Biological effects on flocculation of fine-grained suspended sediment in natural seawater
T
Kristoffer Hofer Skinnebach, Mikkel Fruergaard, Thorbjørn Joest Andersen∗ Department of Geosciences and Natural Resource Management, University of Copenhagen, Øster Voldgade 10, DK-1350, Copenhagen K, Denmark
A R T I C LE I N FO
A B S T R A C T
Keywords: Flocculation Cohesive sediment dynamics Settling experiments Particulate organic matter PCam
The flocculation process is ever occurring in the marine and estuarine environment, and better knowledge of the biological influence as a governing factor is central to improve the understanding and modelling of the horizontal distribution of sediments. In this study we performed a series of laboratory experiments with fine-grained sediments from Sermilik Fjord and Young Sound, situated in Southeast and Northeast Greenland, respectively. The sediment was suspended in natural low-turbidity seawater, filtered seawater and NaCl-supplemented tap water to quantify the isolated effect of particulate organic material (POM) and dissolved substances on flocculation of fine-grained cohesive sediment. A high-resolution camera system (PCam) was applied to observe the effects, and the images and videos were processed in MatLab. The results showed a significantly enhanced flocculation from the presence of POM with larger floc sizes and higher settling velocities compared to flocs formed in seawater filtered with a retention diameter of 0.7 μm. The influences of the remaining dissolved substances, however, led to an enhancement of the flocculation and mass settling of particles compared to those of the control experiments (NaCl-supplemented tap water). The comparison of flocculation potential of sediments from the two different geographic locations in Greenland showed large differences in size and effective density of the flocculated particles, likely caused by the observed differences in texture and organic content of the sediments.
1. Introduction Fine-grained cohesive sediment is rarely found in the form of single particles in natural environments as the particles are typically aggregated into larger particles (e.g. Droppo, 2001). Aggregation of particles suspended in the water column is termed flocculation and the process is governed by numerous parameters and processes including sediment concentration and particle collision (e.g. Eisma et al., 1991; Manning and Dyer, 1999; Winterwerp, 2002; Keyvani and Strom, 2014; Mehta, 2014; Strom and Keyvani, 2016). Flocculation processes are diverse and biological interaction with cohesive sediment of both particulate (POM) and dissolved organic matter (DOM) is important for flocculation efficiency and settling velocity of the particles (e.g. Avnimelech et al., 1982; Alldredge and Gotschalk, 1989; De La Rocha et al., 2008). This mutual dependency between inorganic and organic matter (OM) has implications for example for the effect of inorganic particles on transport of carbon from the atmosphere to the deep sea, the carbon pump (e.g. Passow and De La Rocha, 2006; Iversen and Ploug, 2010), and in the management of harmful algal blooms. The distribution patterns of sediments are, on the other hand, important
∗
from a geoscientific and coastal engineering point of view, and further knowledge about biological effects on particle settling is necessary to improve distribution and sedimentation models. The settling velocity (Ws) of suspended particles is dependent on the size and density of particles as well as the viscosity of the fluid. In typical marine environments Ws is primarily controlled by the size distribution of the flocs in suspension, but the relationship between the two is not linear for flocculated particles. Markussen et al. (2016) for example argued that flocs formed with labile iron (Fe) increased the horizontal transport rather than forcing deposition of the material because of the irregular shape and low density of the resulting macroflocs. Most flocs formed in the natural environment consist of both inorganic and less dense OM resulting in increased porosity and irregular shape of the flocs (Droppo, 2001). The influence of organic matter on flocculation potential was shown by e.g. Mietta et al. (2009) who found limited flocculation of muds in the absence of OM. The organic matter consists of both detritus and living cells. Phytoplankton and microphytobenthos will usual constitute a substantial part of the OM (Underwood and Kromkamp, 1999) and both may produce extracellular polymeric substances (EPS) and transparent exopolymer
Corresponding author. E-mail address: [email protected] (T.J. Andersen).
https://doi.org/10.1016/j.ecss.2019.106395 Received 24 September 2018; Received in revised form 8 July 2019; Accepted 18 September 2019 Available online 19 September 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
particles (TEP) which will tend to stabilize cohesive sediment beds (e.g. Tolhurst et al., 2002; Underwood and Paterson, 2003) and increase flocculation (Wolanski, 2007;Passow, 2002; Zhang et al., 2018). The extent of the flocculation also varies with the microbial activity and other environmental conditions (Lee et al., 2014). This implies a spatial as well as a seasonal variation (Fettweis and Baeye, 2015) in the distribution potential of sediment in estuarine and marine environments governed by the concentrations of phytoplankton, i.e. phytoplankton blooms alter the distribution patterns (). Several laboratory studies have quantified the reduction in algae concentrations by addition of cohesive sediment to the communities due to of flocculation and thereby increased settling of the particles (e.g. Hamm, 2002; Verspagen et al., 2006). However, to the knowledge of the authors, no studies have quantified the isolated effects of phytoplankton on floc characteristics such as size and density and the settling of inorganic particles. The overall aim of the present study is therefore to investigate the effect of POM and dissolved substances in natural seawater on floc properties through systematic laboratory experiments. The specific objectives are to determine: (i) the isolated effects of particulate organic matter (e.g. phytoplankton) on the flocculation of finegrained inorganic particles, (ii) the effects of dissolved substances in natural seawater on the flocculation of fine-grained inorganic particles, and (iii) difference in extent of the flocculation of particles which can be attributed to the composition and texture of the sediment.
Fig. 1. Schematic illustration of the experimental setup: 1) incubation tank, 2) settling column, and 3) bottom tank.
2.2. Camera system and settling chamber The monitoring of settling particles was conducted with an updated version of the PCam particle camera system (Winter et al., 2007; Markussen et al., 2016). This system obtains images with a Canon D70 EOS digital SLR camera having a resolution of 5472 × 3648 pixels and video in Full HD with a resolution of 1920 × 1080 pixels. The camera is contained inside a polyoxymethylene pressure housing with a laser mounted on the outside. The collimated direct diode laser creates a 2 mm thick sheet illuminating the particles in focus with a pixel size of 4.1 μm resulting in a lower detection limit of approx. 10 μm particles corresponding to an area of 4 pixels. See Markussen (2016) for more details about the PCam system. The experiments were carried out using a settling chamber designed for the PCam system (Fig. 1). It consists of three different tanks: 1) the incubation tank, 2) the settling column, and 3) the bottom tank. The incubation tank is cylindrical (Ø: 40 cm, H: 15 cm) and fitted with a paddle, which generates turbulence to prevent the sediment from settling out during the incubation period. A sliding hatch is fitted in the bottom of the tank and is opened manually. The cylindrical settling column (Ø: 15 cm, H: 17 cm) is the pathway guiding the settling particles directly down to the camera position located in the bottom tank (H: 42 cm, L: 34 cm, W: 26 cm).
2. Materials and methods 2.1. Sediment and water The natural sediments used in the present study originates from the bed material of two different fjords in Greenland; Sermilik Fjord and Young Sound (sampling locations latitude 65.8900, longitude −37.8814, water depth 680 m and latitude 74.4343, longitude −20.7573, water depth 280 m respectively). This sediment was chosen because they had very low contents of organic material which could otherwise potentially make the sediments themselves prone to flocculation. Samples from Sermilik were used in the experiments with natural seawater, and samples from Young Sound were used to evaluate the isolated effects of changing texture and content of OM on the flocculation processes. The samples were first ultrasonically dispersed with a Bandelin UW 2200 ultrasonic probe for 2 min and wet sieved through a 20 μm mesh. Subsequently, the fraction < 20 μm were analysed on a Malvern Mastersizer E/2000 to obtain grain-size distributions. The sediment from Sermilik Fjord had a mean grain size of approx. 4 μm and approx. 7 μm for the Young Sound sediment. The Sermilik sediment was used to investigate the effects of POM and DOM in seawater because of the low content of clay minerals and OM, and an analysis of loss on ignition (LOI) showed an OM content of 3.1 ± 0.1%. In comparison, the Young Sound sediment had an OM content of 7.1 ± 0.3%. The seawater was sampled in The Sound (Øresund), Denmark (latitude 55.6936, longitude 12.6186), which is a location with continuous exchange of water between the Kattegat and the Baltic Sea. The characteristics of the water in The Sound can vary on a weekly basis depending on the origin, with more saline water from the Kattegat and brackish water from the Baltic Sea. Low salinities were found during the present campaign with values of approx. 9 PSU. This variation in the origin of the water is also expressed in other characteristics such as nutrient concentrations and amount of OM. The Sound region typically experiences one or two algal blooms in the spring dependent on the amount of sunlight and wind conditions, and a bloom in the autumn when wind-induced mixing of the water column occurs. The algae concentration was estimated by the amount of chl a in the water, which is commonly used as a proxy for the phytoplankton concentration, and by the amount of POM in the water after filtration on 0.7 μm filters.
2.3. Experimental procedure To obtain room temperature (~20 °C) the seawater was stored in darkness for 24 h after sampling before being sieved through a 63 μm mesh to remove large particles that could obscure the images. Fifteen litre of seawater was filtered through three pre-rinsed 47 mm Whatman GF/F glass fibre filters with a 0.7 μm retention diameter to remove all POM (inclusive phytoplankton) (Knap et al., 1996). One of the filters was immediately frozen at −18 °C for later determination of chlorophyll (chl) a content, and one filter was used for determination of POM. Due to the capacity of the instrumental setup and time constraints of each experiment, it was only possible to carry out a single experiment per day, and the filtered seawater was therefore stored in darkness another 24 h. Before each experiment, the salinity and temperature of the seawater was measured to determine its density. The bottom tank was filled with 30 l of tap water mixed with NaCl. The water was mixed to a density of approx. 5 kg m−3 higher than the seawater to prevent advective currents within the settling chamber. Furthermore, the tap water in the bottom tank was kept colder than the water in the incubation chamber to prevent density currents in the settling tank. At the start of incubation 1.4 g of sediment was added to water, yielding a concentration of 100 mg l−1, and incubated under stirring for 2
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
2 h. A rotation speed of 25 rounds per minute (rpm) corresponding to a shear rate (G) of 150 s−1 following calculations from Logan (1999), was found to keep most of the particles in suspension. The turbulence is likely overestimated due to the fact that the incubation chamber is circular and the paddle occupies the entire width of the chamber. The result of this is possibly a reduction in actual turbulence in comparison to the calculated turbulence as the entire water column is effectively moving at a velocity only slightly lower than that of the paddle. Ten pictures were taken prior to opening of the hatch (T0) to obtain information on background noise. Following the opening, 10 pictures were taken over a 30 s period every 5 min followed by a 30 s video. The settling of the particles was observed for 2 h and 15 min. The pictures were used for characterization of the particles (mean equivalent spherical diameter (ESD) and volume concentration (VC)), and the settling velocity was determined from the videos. The combination of pictures and video was used to estimate the effective density of the particles following Stokes’ equation for settling velocity. This equation assumes that the particles are single grains with perfect sphericity, which is rarely the case in neither nature nor our experimental setup. However, the method provides an estimate of the density of the flocs and enables comparison with previously published studies.
Table 1 Measured values of SPMC, POM, LOI, and chlorophyll a from the seawater samples. Sample
SPMC (mg l−1)
POM (mg l−1)
LOI (%)
Chl a (μg l−1)
Seawater 26/4-17 Seawater 2/5-17 Seawater 7/5-17
2.4 1.4 1.0
1.4 0.8 0.6
44 47 44
1.1 2.0 1.4
ESD in unfiltered seawater peaked at 117 μm and reached the camera after 40 min of settling. The mean floc ESD in the filtered treatment reached a maximum of 97 μm, observed after 60 min, whereas the mean floc ESD in the control treatment peaked after 65 min of settling with a size of 76 μm. Overall, the maximum floc ESD with the unfiltered treatment was significantly (p < 0.05) larger than the maximum floc ESD observed with the control treatment, and a difference was observed in floc sizes within all of the three treatments. All treatments showed variability in the floc size distribution when the larger flocs reached the camera position. This is an expression of 1) a difference in the time of observation of the first flocs within the replications, and 2) the very low number of particles observed at this point. As the experiments progressed the variation within the triplicates decreased. Furthermore, a gradual increase in mean floc ESD was observed, which is attributed to presence of a few small, but observable particles in the settling chamber from the beginning of the experiment. These particles caused some noise in the analyses of floc size distribution in the beginning of the experiments, but analysis of the VC indicates their insignificance in the overall transport of material (Fig. 4). The on-going measurements of VC showed that the sedimentation of the total mass was much more rapid in the treatments with seawater.
2.4. Chl a, POM, and picture analysis The Whatman GF/F glass fibre filters (0.7 μm) were stored at −18 °C for up to two weeks before the chl a content was spectrophotometrically determined after extraction with 10 mL 96% ethanol for 24 h at 5 °C in darkness. Subsequently, the samples were centrifuged for 10 min at 2500 rpm. The absorbance was measured at 665 nm and 750 nm both before and after acidification by 0.3 mL of HCl. The chl a content (μg L−1) was determined following Parsons et al. (1984). POM was determined by loss on ignition (LOI) by combustion of the dry GF/F filters at 550 °C for 2 h. The images were analysed in Matlab using a script designed for this setup by Markussen (2016). The script includes several steps to remove noise from the images based on adjustable threshold limits, and yields characteristics of the particles including particle size measured in ESD and VC. The data basis of this study consists of almost 3000 images and 2.5 h of video of settling particles and verification of the analysis was performed by detailed studies of individual images with suspicious yields and random checks. Any images containing misinterpreted particle characteristics (e.g. multiple closely located flocs interpreted as one large floc) were rejected.
3.2. Settling velocities The highest settling velocities were observed with the unfiltered treatment, where the mean floc settling velocity observed after 25 min was 0.33 ± 0.04 m s−1 (Fig. 5). The first measurable flocs in both the filtered and control treatment were observed after 40 min of settling with velocities of 0.24 ± 0.02 m s−1. Ws of the flocs at peak ESD were significantly higher (p < 0.05) in the experiments with unfiltered seawater with a mean velocity of 0.27 ± 0.02 mm s−1 opposed to 0.18 mm s−1 and 0.20 ± 0.01 mm s−1 in the experiments with filtered seawater and the control experiments, respectively. There was insignificant difference in Ws within the treatments for the individual time steps of the experiments.
3. Results
3.3. Sediment comparison
A total of four experiments with triplicates were carried out; three different treatments with sediment from Sermilik and one treatment with sediment from Young Sound. All the results presented here regarding floc characteristics are based on the average of the triplicates with standard deviations, each representing mean values from the pictures taken at each time step. At the time of sampling, the amount of algae in the seawater was low, and the chl a levels were measured in the range of 1.1–2.0 μg l−1, which is consistent with measurements carried out by NOVANA (2017) (0.7 μg l−1 on May 9th, sampled in the Sound north of the sampling site of this study). Furthermore, the analyses showed low concentrations of suspended particulate matter (SPMC) and POM for all three seawater samples (Table 1).
The mean floc ESD for the Young Sound sediment peaked at 108 μm (Fig. 6). Compared to flocs formed from the Sermilik sediment with the same treatment, which peaked at 76 μm even though similar Ws were observed (Fig. 7), suggests a much lower effective density of the flocs (Fig. 9). The mass transportation pattern was similar to that of the Sermilik sediment, but the experiments indicate that the total mass of sediment from Young Sound would have been deposited faster than the Sermilik Fjord sediment if the experiments had lasted longer (Fig. 8). 3.4. Effective density and settling velocity The similarity in Ws combined with the difference in mean floc ESD within the three different treatments suggests a difference in the effective density of the flocculated particles. When plotted as a function of the floc sizes (Fig. 9) there is a clear tendency towards a decrease in effective densities when the floc sizes increased. Furthermore, although some overlap occurs, a segregation of the observations from the
3.1. Floc sizes Regardless of the relatively low levels of chl a, a significant (p < 0.05) difference in floc sizes was observed between the three treatments with the Sermilik sediment (Fig. 2 and Fig. 3). The mean floc 3
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 2. Floc images representing the largest average ESD for each treatment. a) unfiltered seawater, b) filtered seawater, c) control, and d) Young Sound sediment, NaCl-supplemented tap water. Scale bar is 100 μm.
with a mean effective density of 60 kg m−3 averaged over the entire settling experiment. The extent of the mutual flocculation of algae and inorganic particles has been shown to be dependent on both algae species and mineral composition (Kiørboe and Hansen, 1993; Hamm, 2002; Turner and Millward, 2002), and flocculation times from minutes to hours have been reported from both laboratory studies (Verspagen et al., 2006) and field investigations (Milligan, 1995; Mikkelsen and Pejrup, 2000). Our results show that enhanced and rapid flocculation takes place even in low turbidity water and with chl a concentrations in the order of only 1 to 2 μg l−1. The experimental setup allows measurements of both size and settling velocity and estimation of effective densities of the resulting flocs thereby demonstrating that the particulate organic matter results in increased floc size but a decrease in effective density compared to experiments with filtered seawater and the control experiments. The study therefore highlights the importance of measurement of both floc size and settling velocity as estimation of the settling velocity based only on the floc size would likely results in overestimation of the settling velocity due to the systematic variation in effective density. The variations in flocculation efficiency makes it difficult to model the effects of phytoplankton on the distribution potential of sediments in the natural environment, because of the large number and diversity of phytoplankton groups and species and the variations in the chemical composition of marine and estuarine environments. However, the present experiments provide strong indications of significant flocculation due to the presence of phytoplankton alone. This in turn results in reduced horizontal transportation of the particles. Calculation of fractal dimension has not been attempted on the basis of the present data-set as the diversity of flocculation mechanisms in
different treatments is observed with flocs formed in unfiltered seawater being the largest and least dense, and flocs formed in NaCl-supplemented tap water being the smallest but generally more dense. The flocs formed from the Young Sound sediment in NaCl-supplemented tap water, however, are the least dense. The results from the present study fall well within the same area when plotted together with regressions of previous findings, of which the majority are in-situ investigations (Fig. 9). A plot of settling velocity versus mean floc size for all treatments is shown in Fig. 10 together with regression lines from some of the studies shown in Fig. 9 and two other studies. Fennessy et al. (1994) does not provide a regression equation on their settling velocity data (Fig. 6 in their paper) but the present data show a relationship quite similar to their data and the study by Mikkelsen and Pejrup (2001). The remaining studies found somewhat higher settling velocities in relation to floc size.
4. Discussion The present investigation demonstrates that flocculation efficiency is significantly higher in natural seawater than in filtered seawater with no or very little organic content, pointing to the influence of particulate organic matter on the settling of fine-grained minerogenic sediment. The effect was observed despite the low organic content of around 3% of the sediment. The flocs formed in unfiltered seawater showed a mean ESD of 117 μm as maximum, but flocs of more than 150 μm were observed during the experiments. The flocs in unfiltered seawater also exhibited the highest settling velocities of 0.33 ± 0.04 mm s-1, but were in general less dense than the flocs formed in the other treatments,
Fig. 3. Mean floc equivalent spherical diameter (ESD) for all three treatments with Sermilik sediment. 4
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 4. Volume concentrations (VC) for all three treatments with Sermilik sediment.
likely fundamental differences in the aggregation dynamics between high- and low-turbidity environments. These differences are likely also responsible for some of the scattering of the regression lines shown in Figs. 9 and 10. By filtration with the Whatman GF/F glass fibre filters with a 0.7 μm retention diameter the water is depleted of all POM, and the experiments showed that flocculation efficiency had visibly decreased compared to the experiments with unfiltered seawater. The flocs now showed a peak mean ESD of 97 μm with observed maximum sizes of about 110 μm. Ws was significantly lower even though the mean effective density generally was higher with an average 65 kg m−3. This highlights the importance of floc size on settling velocity, but it also suggests that the composition of the flocs were different. The result indicates that the presence of POM increases the porosity and thereby water content of the flocs, but electron microscopy images are necessary to determine the structure in more detail. In-situ investigations during diatom blooms have revealed macroflocs of several millimeters
natural suspensions with organic materials and biological processes is large. For example, fecal pellets produced by copepods, mussels and fish will be a significant contribution to the suspended load in many environments but they obviously do not flocculate into aggregates with similar characteristics. The aggregates found in suspension may also be formed at the bed as indicated by Forsberg et al. (2018) who showed how aggregation at the bed produced aggregates which are likely to constitute a substantial part of the “microfloc” population observed in many studies. It is not likely that the subsequent flocculation of microflocs in the water column into macro-flocs will produce flocs with similar characteristics and fractal dimensions as those formed at the sediment bed. However, fractal dimension may be a meaningful concept in some cases, for example when dealing with flocculation in highturbidity settings (e.g. Winterwerp et al., 2006) where flocculation in the water column will be dominating the aggregation processes. This is in contrast to low-turbidity settings where bioaggregates and biologically induced flocculation is likely to dominate and there is therefore
Fig. 5. Settling velocities measured for all three treatments with Sermilik sediment. The black line indicates the calculated settling velocity, Ws calc. (settling distance/settling time). 5
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 6. Comparison of mean floc equivalent spherical diameter (ESD) from Sermilik and Young Sound sediment treated with NaCl-supplemented tap water.
was observed in the particle ESD as well as in the VC (Figs. 3 and 4). This suggests a more rapid sedimentation of the entire sediment pool in the presence of DOM, which can contribute to large spatial and seasonal differences in sediment distribution and sedimentation patterns due to varying contents of DOM. The experiments with sediments from two fjord sites with different texture, minerogenic composition and OM content revealed significant variations in flocculation efficiency. The flocs formed from Young Sound sediment in NaCl-supplemented tap water was similar to flocs formed from the Sermilik sediment in filtered seawater regarding mean floc ESD, but the sedimentation rate was lower indicating a lower effective density (average of 33 kg m−3) of the flocs. However, the sedimentation rate of the Young Sound sediment was higher than the Sermilik sediment in NaCl-supplemented tap water, with significantly larger flocs. The exact reason for this difference is not known, but is likely caused by the slightly coarser primary particle distribution and the larger OM content of the sediment from Young Sound. Mineral composition may also play a role and this will be the subject of future
(Kranck and Milligan, 1988) and increases in settling velocity of two orders of magnitude (Alldredge and Gotschalk, 1989). Those flocs, however, were formed under low levels of shearing and with high levels of chl a (i.e. high concentrations of phytoplankton), which contrast with the conditions of the present investigation. Visible difference in flocculation extent was nonetheless found in this study, which illustrates the potential difference in distribution patterns of fine-grained sediment in seasonal transition periods, with less horizontal transport and more rapid sedimentation induced by POM. The presence of algae amplifies the flocculation processes, but dissolved substances alone have also been shown to enhance the process (e.g. De La Rocha et al., 2008; Markussen et al., 2016). The majority of the carbon pool in many aquatic environments is in dissolved form and may originate from for example microbial activity (e.g. reminiscences from an algae bloom) or from terrestrial washout (Thurman, 1985). The effect of DOM is shown by comparison of the flocs formed in filtered seawater to the flocs formed in NaCl-supplemented tap water. The two treatments exhibited similar settling velocities, but a clear difference
Fig. 7. Comparison of settling velocities (Ws) from Sermilik and Young Sound sediment treated with NaCl-supplemented tap water. The black line indicates the calculated settling velocity, Ws calc. (settling distance/settling time). 6
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 8. Comparison of volume concentrations (VC) from Sermilik and Young Sound sediment treated with NaCl-supplemented tap water.
studies. Mietta et al. (2009) observed an increase in floc sizes directly linked to the OM in the sediment, but similarly to the present study, the composition of the OM was not further investigated. The present investigation relies on laboratory experiments, but the materials used are all sampled in natural environments, and the findings can therefore be expected to be within the range of what can be observed in nature. However, some modifications were necessary in order to complete the experiments. Most importantly, the seawater samples were left in darkness for 24 h in order to obtain room temperature. When phytoplankton is exposed to complete darkness for a longer period, the cells will compensate by increased production of chl a and decreased growth (Jakobsen et al., 2012). Growth limitation is furthermore associated with an increase in the secretion of EPS (Thornton, 2002), which can play a dominant role in flocculation of particles (Droppo, 2001). However, the measured levels of chl a corresponded well to in-situ observations at the sampling site (NOVANA, 2017), which also showed that the sampling took place following a period of increased chl a levels indicating a phytoplankton bloom. Despite the low levels of chl a and POM, a clear difference was found between experiments with unfiltered and filtered seawater, which is
attributed to the presence of phytoplankton, even in very low concentrations. Even though the biological and chemical characteristics of the seawater might have been altered through the procedure used in the present investigation, the PCam system and the designated settling chamber offer a unique possibility to investigate isolated effects of different parameters of the flocculation process in high detail and under natural-like conditions in the laboratory or in-situ. Future studies should include an in-depth investigation of the chemical and biological composition of the water in which the flocs are formed, especially concerning algal species and cell counts. Such studies would contribute with further quantitative knowledge regarding the distribution and sedimentation of fine-grained cohesive sediments. 5. Conclusions Through a number of experiments, a particle camera system (PCam) was used to quantify the effects of particulate and dissolved substances present in low-turbidity natural seawater on flocculation of fine-grained cohesive sediment. Flocs formed in unfiltered seawater were Fig. 9. The calculated effective density as a function of mean floc equivalent spherical diameter (ESD). Blue dots: unfiltered seawater, green dots: filtered seawater, red dots: control, crosses: Young Sound sediment. The lines show results from previous investigations (Al Ani et al., 1991; Fennessy et al., 1994; Manning and Dyer, 1999; Mikkelsen and Pejrup, 2001; Markussen and Andersen, 2013). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
7
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 10. The settling velocity as a function of floc size. Blue dots: unfiltered seawater, green dots: filtered seawater, red dots: control, crosses: Young Sound sediment. The lines show results from previous investigations (Gibbs, 1985; Manning and Dyer, 1999; Mikkelsen and Pejrup, 2001; Agrawal and Pottsmith, 2000). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
significantly (p < 0.05) larger than flocs formed in NaCl-supplemented tap water. The settling velocities were similarly higher and the sedimentation of the total sediment volume was much more rapid. Through approximations by chlorophyll a levels and particulate organic matter (POM) content it is concluded that the concentration of algae in the seawater was low at the time of sampling, but both floc size and settling velocity was nevertheless increased in the presence of the algae. It was also shown that flocculation of particles was enhanced in seawater even when plankton (phyto- and zoo-) was removed compared to control experiments with NaCl-supplemented tap water. This suggests a tangible effect on the process induced by bacteria, dissolved orga nic matter, and/or chemical compounds. The present study further shows that sediment characteristics are of importance concerning the flocculation potential. More organic-rich and slightly coarser sediment formed larger, but less dense flocs than sediment with lower organic matter content.
Oceans 120, 5648–5667. Forsberg, P.L., Skinnebach, K.H., Becker, M., Kroon, A., Andersen, T.J., 2018. The influence of aggregation on cohesive sediment erosion and settling. Cont. Shelf Res. 171, 52–62. Gibbs, R.J., 1985. Estuarine flocs: their size, settling velocity and density. J. Geophys. Res. 90, 3249–3251. Hamm, C.E., 2002. Interactive aggregation and sedimentation of diatoms and clay-sized lithogenic material. Limnol. Oceanogr. 47, 1790–1795. Iversen, M.H., Ploug, H., 2010. Ballast minerals and the sinking carbon flux in the ocean: carbon-specific respiration rates and sinking velocity of marine snow aggregates. Biogeosciences 7 (9), 2613–2624. Jakobsen, R., Hansen, P.J., Daugbjerg, N., Andersen, N.G., 2012. The fish-killing dictyochophyte Pseudochattonella farcimen: adaptations leading to bloom formation during early spring in Scandinavian waters. Harmful Algae 18, 84–95. Keyvani, A., Strom, K., 2014. Influence of cycles of high and low turbulent shear on the growth rate and equilibrium size of mud flocs. Mar. Geol. 354, 1–14. Kiørboe, T., Hansen, J.L.S., 1993. Phytoplankton aggregate formation: observations of patterns and mechanisms of cell sticking and the significance of exopolymeric particles. J. Plankton Res. 15, 993–1018. Protocols for the joint global ocean flux study (JGOFS) core measurements. JGOFS Report Nr. vol. 19, vi+170 pp In: Knap, A., Michaels, A., Close, A., Ducklow, H., Dickson, A. (Eds.), Reprint of the IOC Manuals and Guides No. 29. UNESCO 1994. Kranck, K., Milligan, T., 1988. Macroflocs from diatoms: in situ photography of particles in bedford basin, nova scotia. Mar. Ecol. Prog. Ser. 44, 183–189. Lee, B.J., Toorman, E., Fettweis, M., 2014. Multimodal particle size distributions of finegrained sediments: mathematical modeling and field investigation. Ocean Dyn. 64, 429–441. Logan, B.E., 1999. Environmental Transport Processes. John Wiley & Sons, Hoboken, N. J., pp. 654. Manning, A.J., Dyer, K.R., 1999. A laboratory examination of floc characteristics with regard to turbulent shearing. Mar. Geol. 160, 147–170. Markussen, T.N., Andersen, T.J., 2013. A simple method for calculating in situ floc settling velocities based on effective density functions. Mar. Geol. 344, 10–18. Markussen, T.N., Elberling, B., Winter, C., Andersen, T.J., 2016. Flocculated meltwater particles control Arctic land-sea fluxes of labile iron. Sci. Rep. 6, 24033. Markussen, T.N., 2016. Parchar – characterization of suspended particles through image processing in Matlab. J. Open Res. Softw. 4 (1), e26. Mehta, A.J., 2014. An Introduction to Hydraulics of Fine Sediment Transport. Advanced Series on Ocean Engineering, vol. 38 World Scientific Publishing Co, Hackensack, NJ. Mietta, F., Chassange, C., Manning, A.J., Winterwerp, J.C., 2009. Influence of shear rate, organic matter content, pH and salinity on mud flocculation. Ocean Dyn. 59, 751–763. Mikkelsen, O.A., Pejrup, M., 2000. In situ particle size spectra and density of particle aggregates in a dredging plume. Mar. Geol. 170, 443–459. Mikkelsen, O.A., Pejrup, M., 2001. The use of a LISST-100 laser particle sizer for in-situ estimates of floc size, density and settling velocity. Geo Mar. Lett. 20, 187–195. Milligan, T., 1995. An examination of the settling behavior of a flocculated suspension. Neth. J. Sea Res. 33, 163–171. NOVANA, 2017. Det Nationale Program for Overvågning Af Vandmiljøet Og Naturen. WWW Page. http://havudsigten.dk/en/ensemble/oresund last visited on 28/02-19. Parsons, T.R., Maita, Y., Lalli, C.M., 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon, pp. 173. Passow, U., 2002. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55, 287–333. Passow, U., De La Rocha, C.L., 2006. Accumulation of mineral ballast on organic aggregates. Glob. Biogeochem. Cycles 20 (1), GB1013. Strom, K., Keyvani, A., 2016. Flocculation in a decaying shear field and its implications
Acknowledgement The authors would like to thank Thor Nygaard Markussen for constructive discussions, development and modification of the Matlab script. Comments and suggestions by two anomous reviewers were also greatly appreciated. This work was supported by the Velux Foundations, grant nos. 17668 and 18533. References Agrawal, Y.C., Pottsmith, H.C., 2000. Instruments for particle size and settling velocity observations in sediment transport. Mar. Geol. 168, 89–114. Al Ani, S., Dyer, K.R., Huntley, D.A., 1991. Measurement of the influence of salinity on floc density and strength. Geo Mar. Lett. 11, 154–158. Alldredge, A.L., Gotschalk, C.C., 1989. Direct observation of the mass flocculation of diatom blooms – characteristics, settling velocity and formation of diatom aggregates. Deep-Sea Res. Part A: Oceanograph. Res. Papers 36 (2), 159–171. Avnimelech, Y., Troeger, B.W., Reed, L.W., 1982. Mutual flocculation of algae and clay: evidence and implications. Science 216, 63–65. De La Rocha, C.L., Nowald, N., Passow, U., 2008. Interactions between diatom aggregates, minerals, particulate organic carbon, and dissolved organic matter: further implications for the ballast hypothesis. Glob. Biogeochem. Cycles 22 (4), GB4005. Droppo, I.G., 2001. Rethinking what constitutes suspended sediment. Hydrol. Process. 15 (9), 1551–1564. Eisma, D., Bernard, P., Cadee, G., Ittekkot, V., Kalf, J., Laane, R., Martin, J., Mook, W., van Put, A., Schuhmacher, T., 1991. Suspended-matter particle size in some WestEuropean estuaries; Part II: a review on floc formation and break-up. Neth. J. Sea Res. 28 (3), 215–220. Fennessy, M.J., Dyer, K.R., Huntley, D.A., 1994. INSSEV: an instrument to measure the size and settling velocity of flocs in situ. Mar. Geol. 117, 107–117. Fettweis, M., Baeye, M., 2015. Seasonal variation in concentration, size, and settling velocity of muddy marine flocs in the benthic boundary layer. J. Geophys. Res.:
8
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Verspagen, J.M.H., Visser, P.M., Huisman, J., 2006. Aggregation with clay causes sedimentation of the buoyant cyanobateria Mycrocystis spp. Aquat. Microb. Ecol. 44, 154–174. Winter, C., Becker, M., Ernstsen, V.B., Hebbeln, D., Port, A., Bartholoma, A., Lunau, M., 2007. In-situ observation of aggregate dynamics in a tidal channel using acoustics, laser diffraction and optics. J. Coast. Res. SI 50, 1173–1177. Winterwerp, J.C., 2002. On the flocculation and settling velocity of estuarine mud. Cont. Shelf Res. 22 (9), 1339–1360. Winterwerp, J.C., Manning, A.J., Martens, C., de Mulder, T., Vanlede, J., 2006. A heuristic formula for turbulence-induced flocculation of cohesive sediment. Estuar. Coast Shelf Sci. 68, 195–207. Wolanski, E., 2007. Estuarine Ecohydrology, Chapter 3. Elsevier, Amsterdam, The Netherlands. Zhang, N., Thompson, C.E.L., Townend, I.H., Rankin, K.E., Paterson, D.M., Manning, A.J., 2018. Nondestructive 3D imaging and quantification of hydrated biofilm-sediment aggregates using X-ray microcomputed tomography. Environ. Sci. Technol. 52, 13306–13313. https://doi.org/10.1021/acs.est.8b03997.
for mud removal in near-field river mouth discharges. J. Geophys. Res.: Oceans 121, 2142–2162. Thornton, D.C.O., 2002. Diatom aggregation in the sea: mechanisms and ecological implications. Eur. J. Phycol. 37 (2), 149–161. Thurman, E.M., 1985. Organic Geochemistry of Natural Waters. Kluwer Academic, pp. 497. Tolhurst, T.J., Gust, G., Paterson, D.M., 2002. The influence on an extra-cellular polymeric substance (EPS) on cohesive sediment stability. In: Winterwerp, J.C., Kranenburg, C. (Eds.), Fine Sediment Dynamics in the Marine Environment – Proceedings in Marine Science 5. Elsevier, Amsterdam, pp. 409–425. Turner, A., Millward, G.E., 2002. Suspended particles: their role in estuarine biogeochemical cycles. Estuar. Coast Shelf Sci. 55 (6), 857–883. Underwood, G.J.C., Kromkamp, J., 1999. Primary production by phytoplankton and microphytobenthos in estuaries. Adv. Ecol. Res. 29, 93–153. Underwood, G.J.C., Paterson, D.M., 2003. The Importance of Extracellular Carbohydrate Production by Marine Epipelic Diatoms. Advances in Botanical Research (Incorporating Advances in Plant Pathology), vol. 40. Elsevier, Amsterdam, pp. 183–240.
9
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Biological effects on flocculation of fine-grained suspended sediment in natural seawater
T
Kristoffer Hofer Skinnebach, Mikkel Fruergaard, Thorbjørn Joest Andersen∗ Department of Geosciences and Natural Resource Management, University of Copenhagen, Øster Voldgade 10, DK-1350, Copenhagen K, Denmark
A R T I C LE I N FO
A B S T R A C T
Keywords: Flocculation Cohesive sediment dynamics Settling experiments Particulate organic matter PCam
The flocculation process is ever occurring in the marine and estuarine environment, and better knowledge of the biological influence as a governing factor is central to improve the understanding and modelling of the horizontal distribution of sediments. In this study we performed a series of laboratory experiments with fine-grained sediments from Sermilik Fjord and Young Sound, situated in Southeast and Northeast Greenland, respectively. The sediment was suspended in natural low-turbidity seawater, filtered seawater and NaCl-supplemented tap water to quantify the isolated effect of particulate organic material (POM) and dissolved substances on flocculation of fine-grained cohesive sediment. A high-resolution camera system (PCam) was applied to observe the effects, and the images and videos were processed in MatLab. The results showed a significantly enhanced flocculation from the presence of POM with larger floc sizes and higher settling velocities compared to flocs formed in seawater filtered with a retention diameter of 0.7 μm. The influences of the remaining dissolved substances, however, led to an enhancement of the flocculation and mass settling of particles compared to those of the control experiments (NaCl-supplemented tap water). The comparison of flocculation potential of sediments from the two different geographic locations in Greenland showed large differences in size and effective density of the flocculated particles, likely caused by the observed differences in texture and organic content of the sediments.
1. Introduction Fine-grained cohesive sediment is rarely found in the form of single particles in natural environments as the particles are typically aggregated into larger particles (e.g. Droppo, 2001). Aggregation of particles suspended in the water column is termed flocculation and the process is governed by numerous parameters and processes including sediment concentration and particle collision (e.g. Eisma et al., 1991; Manning and Dyer, 1999; Winterwerp, 2002; Keyvani and Strom, 2014; Mehta, 2014; Strom and Keyvani, 2016). Flocculation processes are diverse and biological interaction with cohesive sediment of both particulate (POM) and dissolved organic matter (DOM) is important for flocculation efficiency and settling velocity of the particles (e.g. Avnimelech et al., 1982; Alldredge and Gotschalk, 1989; De La Rocha et al., 2008). This mutual dependency between inorganic and organic matter (OM) has implications for example for the effect of inorganic particles on transport of carbon from the atmosphere to the deep sea, the carbon pump (e.g. Passow and De La Rocha, 2006; Iversen and Ploug, 2010), and in the management of harmful algal blooms. The distribution patterns of sediments are, on the other hand, important
∗
from a geoscientific and coastal engineering point of view, and further knowledge about biological effects on particle settling is necessary to improve distribution and sedimentation models. The settling velocity (Ws) of suspended particles is dependent on the size and density of particles as well as the viscosity of the fluid. In typical marine environments Ws is primarily controlled by the size distribution of the flocs in suspension, but the relationship between the two is not linear for flocculated particles. Markussen et al. (2016) for example argued that flocs formed with labile iron (Fe) increased the horizontal transport rather than forcing deposition of the material because of the irregular shape and low density of the resulting macroflocs. Most flocs formed in the natural environment consist of both inorganic and less dense OM resulting in increased porosity and irregular shape of the flocs (Droppo, 2001). The influence of organic matter on flocculation potential was shown by e.g. Mietta et al. (2009) who found limited flocculation of muds in the absence of OM. The organic matter consists of both detritus and living cells. Phytoplankton and microphytobenthos will usual constitute a substantial part of the OM (Underwood and Kromkamp, 1999) and both may produce extracellular polymeric substances (EPS) and transparent exopolymer
Corresponding author. E-mail address: [email protected] (T.J. Andersen).
https://doi.org/10.1016/j.ecss.2019.106395 Received 24 September 2018; Received in revised form 8 July 2019; Accepted 18 September 2019 Available online 19 September 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
particles (TEP) which will tend to stabilize cohesive sediment beds (e.g. Tolhurst et al., 2002; Underwood and Paterson, 2003) and increase flocculation (Wolanski, 2007;Passow, 2002; Zhang et al., 2018). The extent of the flocculation also varies with the microbial activity and other environmental conditions (Lee et al., 2014). This implies a spatial as well as a seasonal variation (Fettweis and Baeye, 2015) in the distribution potential of sediment in estuarine and marine environments governed by the concentrations of phytoplankton, i.e. phytoplankton blooms alter the distribution patterns (). Several laboratory studies have quantified the reduction in algae concentrations by addition of cohesive sediment to the communities due to of flocculation and thereby increased settling of the particles (e.g. Hamm, 2002; Verspagen et al., 2006). However, to the knowledge of the authors, no studies have quantified the isolated effects of phytoplankton on floc characteristics such as size and density and the settling of inorganic particles. The overall aim of the present study is therefore to investigate the effect of POM and dissolved substances in natural seawater on floc properties through systematic laboratory experiments. The specific objectives are to determine: (i) the isolated effects of particulate organic matter (e.g. phytoplankton) on the flocculation of finegrained inorganic particles, (ii) the effects of dissolved substances in natural seawater on the flocculation of fine-grained inorganic particles, and (iii) difference in extent of the flocculation of particles which can be attributed to the composition and texture of the sediment.
Fig. 1. Schematic illustration of the experimental setup: 1) incubation tank, 2) settling column, and 3) bottom tank.
2.2. Camera system and settling chamber The monitoring of settling particles was conducted with an updated version of the PCam particle camera system (Winter et al., 2007; Markussen et al., 2016). This system obtains images with a Canon D70 EOS digital SLR camera having a resolution of 5472 × 3648 pixels and video in Full HD with a resolution of 1920 × 1080 pixels. The camera is contained inside a polyoxymethylene pressure housing with a laser mounted on the outside. The collimated direct diode laser creates a 2 mm thick sheet illuminating the particles in focus with a pixel size of 4.1 μm resulting in a lower detection limit of approx. 10 μm particles corresponding to an area of 4 pixels. See Markussen (2016) for more details about the PCam system. The experiments were carried out using a settling chamber designed for the PCam system (Fig. 1). It consists of three different tanks: 1) the incubation tank, 2) the settling column, and 3) the bottom tank. The incubation tank is cylindrical (Ø: 40 cm, H: 15 cm) and fitted with a paddle, which generates turbulence to prevent the sediment from settling out during the incubation period. A sliding hatch is fitted in the bottom of the tank and is opened manually. The cylindrical settling column (Ø: 15 cm, H: 17 cm) is the pathway guiding the settling particles directly down to the camera position located in the bottom tank (H: 42 cm, L: 34 cm, W: 26 cm).
2. Materials and methods 2.1. Sediment and water The natural sediments used in the present study originates from the bed material of two different fjords in Greenland; Sermilik Fjord and Young Sound (sampling locations latitude 65.8900, longitude −37.8814, water depth 680 m and latitude 74.4343, longitude −20.7573, water depth 280 m respectively). This sediment was chosen because they had very low contents of organic material which could otherwise potentially make the sediments themselves prone to flocculation. Samples from Sermilik were used in the experiments with natural seawater, and samples from Young Sound were used to evaluate the isolated effects of changing texture and content of OM on the flocculation processes. The samples were first ultrasonically dispersed with a Bandelin UW 2200 ultrasonic probe for 2 min and wet sieved through a 20 μm mesh. Subsequently, the fraction < 20 μm were analysed on a Malvern Mastersizer E/2000 to obtain grain-size distributions. The sediment from Sermilik Fjord had a mean grain size of approx. 4 μm and approx. 7 μm for the Young Sound sediment. The Sermilik sediment was used to investigate the effects of POM and DOM in seawater because of the low content of clay minerals and OM, and an analysis of loss on ignition (LOI) showed an OM content of 3.1 ± 0.1%. In comparison, the Young Sound sediment had an OM content of 7.1 ± 0.3%. The seawater was sampled in The Sound (Øresund), Denmark (latitude 55.6936, longitude 12.6186), which is a location with continuous exchange of water between the Kattegat and the Baltic Sea. The characteristics of the water in The Sound can vary on a weekly basis depending on the origin, with more saline water from the Kattegat and brackish water from the Baltic Sea. Low salinities were found during the present campaign with values of approx. 9 PSU. This variation in the origin of the water is also expressed in other characteristics such as nutrient concentrations and amount of OM. The Sound region typically experiences one or two algal blooms in the spring dependent on the amount of sunlight and wind conditions, and a bloom in the autumn when wind-induced mixing of the water column occurs. The algae concentration was estimated by the amount of chl a in the water, which is commonly used as a proxy for the phytoplankton concentration, and by the amount of POM in the water after filtration on 0.7 μm filters.
2.3. Experimental procedure To obtain room temperature (~20 °C) the seawater was stored in darkness for 24 h after sampling before being sieved through a 63 μm mesh to remove large particles that could obscure the images. Fifteen litre of seawater was filtered through three pre-rinsed 47 mm Whatman GF/F glass fibre filters with a 0.7 μm retention diameter to remove all POM (inclusive phytoplankton) (Knap et al., 1996). One of the filters was immediately frozen at −18 °C for later determination of chlorophyll (chl) a content, and one filter was used for determination of POM. Due to the capacity of the instrumental setup and time constraints of each experiment, it was only possible to carry out a single experiment per day, and the filtered seawater was therefore stored in darkness another 24 h. Before each experiment, the salinity and temperature of the seawater was measured to determine its density. The bottom tank was filled with 30 l of tap water mixed with NaCl. The water was mixed to a density of approx. 5 kg m−3 higher than the seawater to prevent advective currents within the settling chamber. Furthermore, the tap water in the bottom tank was kept colder than the water in the incubation chamber to prevent density currents in the settling tank. At the start of incubation 1.4 g of sediment was added to water, yielding a concentration of 100 mg l−1, and incubated under stirring for 2
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
2 h. A rotation speed of 25 rounds per minute (rpm) corresponding to a shear rate (G) of 150 s−1 following calculations from Logan (1999), was found to keep most of the particles in suspension. The turbulence is likely overestimated due to the fact that the incubation chamber is circular and the paddle occupies the entire width of the chamber. The result of this is possibly a reduction in actual turbulence in comparison to the calculated turbulence as the entire water column is effectively moving at a velocity only slightly lower than that of the paddle. Ten pictures were taken prior to opening of the hatch (T0) to obtain information on background noise. Following the opening, 10 pictures were taken over a 30 s period every 5 min followed by a 30 s video. The settling of the particles was observed for 2 h and 15 min. The pictures were used for characterization of the particles (mean equivalent spherical diameter (ESD) and volume concentration (VC)), and the settling velocity was determined from the videos. The combination of pictures and video was used to estimate the effective density of the particles following Stokes’ equation for settling velocity. This equation assumes that the particles are single grains with perfect sphericity, which is rarely the case in neither nature nor our experimental setup. However, the method provides an estimate of the density of the flocs and enables comparison with previously published studies.
Table 1 Measured values of SPMC, POM, LOI, and chlorophyll a from the seawater samples. Sample
SPMC (mg l−1)
POM (mg l−1)
LOI (%)
Chl a (μg l−1)
Seawater 26/4-17 Seawater 2/5-17 Seawater 7/5-17
2.4 1.4 1.0
1.4 0.8 0.6
44 47 44
1.1 2.0 1.4
ESD in unfiltered seawater peaked at 117 μm and reached the camera after 40 min of settling. The mean floc ESD in the filtered treatment reached a maximum of 97 μm, observed after 60 min, whereas the mean floc ESD in the control treatment peaked after 65 min of settling with a size of 76 μm. Overall, the maximum floc ESD with the unfiltered treatment was significantly (p < 0.05) larger than the maximum floc ESD observed with the control treatment, and a difference was observed in floc sizes within all of the three treatments. All treatments showed variability in the floc size distribution when the larger flocs reached the camera position. This is an expression of 1) a difference in the time of observation of the first flocs within the replications, and 2) the very low number of particles observed at this point. As the experiments progressed the variation within the triplicates decreased. Furthermore, a gradual increase in mean floc ESD was observed, which is attributed to presence of a few small, but observable particles in the settling chamber from the beginning of the experiment. These particles caused some noise in the analyses of floc size distribution in the beginning of the experiments, but analysis of the VC indicates their insignificance in the overall transport of material (Fig. 4). The on-going measurements of VC showed that the sedimentation of the total mass was much more rapid in the treatments with seawater.
2.4. Chl a, POM, and picture analysis The Whatman GF/F glass fibre filters (0.7 μm) were stored at −18 °C for up to two weeks before the chl a content was spectrophotometrically determined after extraction with 10 mL 96% ethanol for 24 h at 5 °C in darkness. Subsequently, the samples were centrifuged for 10 min at 2500 rpm. The absorbance was measured at 665 nm and 750 nm both before and after acidification by 0.3 mL of HCl. The chl a content (μg L−1) was determined following Parsons et al. (1984). POM was determined by loss on ignition (LOI) by combustion of the dry GF/F filters at 550 °C for 2 h. The images were analysed in Matlab using a script designed for this setup by Markussen (2016). The script includes several steps to remove noise from the images based on adjustable threshold limits, and yields characteristics of the particles including particle size measured in ESD and VC. The data basis of this study consists of almost 3000 images and 2.5 h of video of settling particles and verification of the analysis was performed by detailed studies of individual images with suspicious yields and random checks. Any images containing misinterpreted particle characteristics (e.g. multiple closely located flocs interpreted as one large floc) were rejected.
3.2. Settling velocities The highest settling velocities were observed with the unfiltered treatment, where the mean floc settling velocity observed after 25 min was 0.33 ± 0.04 m s−1 (Fig. 5). The first measurable flocs in both the filtered and control treatment were observed after 40 min of settling with velocities of 0.24 ± 0.02 m s−1. Ws of the flocs at peak ESD were significantly higher (p < 0.05) in the experiments with unfiltered seawater with a mean velocity of 0.27 ± 0.02 mm s−1 opposed to 0.18 mm s−1 and 0.20 ± 0.01 mm s−1 in the experiments with filtered seawater and the control experiments, respectively. There was insignificant difference in Ws within the treatments for the individual time steps of the experiments.
3. Results
3.3. Sediment comparison
A total of four experiments with triplicates were carried out; three different treatments with sediment from Sermilik and one treatment with sediment from Young Sound. All the results presented here regarding floc characteristics are based on the average of the triplicates with standard deviations, each representing mean values from the pictures taken at each time step. At the time of sampling, the amount of algae in the seawater was low, and the chl a levels were measured in the range of 1.1–2.0 μg l−1, which is consistent with measurements carried out by NOVANA (2017) (0.7 μg l−1 on May 9th, sampled in the Sound north of the sampling site of this study). Furthermore, the analyses showed low concentrations of suspended particulate matter (SPMC) and POM for all three seawater samples (Table 1).
The mean floc ESD for the Young Sound sediment peaked at 108 μm (Fig. 6). Compared to flocs formed from the Sermilik sediment with the same treatment, which peaked at 76 μm even though similar Ws were observed (Fig. 7), suggests a much lower effective density of the flocs (Fig. 9). The mass transportation pattern was similar to that of the Sermilik sediment, but the experiments indicate that the total mass of sediment from Young Sound would have been deposited faster than the Sermilik Fjord sediment if the experiments had lasted longer (Fig. 8). 3.4. Effective density and settling velocity The similarity in Ws combined with the difference in mean floc ESD within the three different treatments suggests a difference in the effective density of the flocculated particles. When plotted as a function of the floc sizes (Fig. 9) there is a clear tendency towards a decrease in effective densities when the floc sizes increased. Furthermore, although some overlap occurs, a segregation of the observations from the
3.1. Floc sizes Regardless of the relatively low levels of chl a, a significant (p < 0.05) difference in floc sizes was observed between the three treatments with the Sermilik sediment (Fig. 2 and Fig. 3). The mean floc 3
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 2. Floc images representing the largest average ESD for each treatment. a) unfiltered seawater, b) filtered seawater, c) control, and d) Young Sound sediment, NaCl-supplemented tap water. Scale bar is 100 μm.
with a mean effective density of 60 kg m−3 averaged over the entire settling experiment. The extent of the mutual flocculation of algae and inorganic particles has been shown to be dependent on both algae species and mineral composition (Kiørboe and Hansen, 1993; Hamm, 2002; Turner and Millward, 2002), and flocculation times from minutes to hours have been reported from both laboratory studies (Verspagen et al., 2006) and field investigations (Milligan, 1995; Mikkelsen and Pejrup, 2000). Our results show that enhanced and rapid flocculation takes place even in low turbidity water and with chl a concentrations in the order of only 1 to 2 μg l−1. The experimental setup allows measurements of both size and settling velocity and estimation of effective densities of the resulting flocs thereby demonstrating that the particulate organic matter results in increased floc size but a decrease in effective density compared to experiments with filtered seawater and the control experiments. The study therefore highlights the importance of measurement of both floc size and settling velocity as estimation of the settling velocity based only on the floc size would likely results in overestimation of the settling velocity due to the systematic variation in effective density. The variations in flocculation efficiency makes it difficult to model the effects of phytoplankton on the distribution potential of sediments in the natural environment, because of the large number and diversity of phytoplankton groups and species and the variations in the chemical composition of marine and estuarine environments. However, the present experiments provide strong indications of significant flocculation due to the presence of phytoplankton alone. This in turn results in reduced horizontal transportation of the particles. Calculation of fractal dimension has not been attempted on the basis of the present data-set as the diversity of flocculation mechanisms in
different treatments is observed with flocs formed in unfiltered seawater being the largest and least dense, and flocs formed in NaCl-supplemented tap water being the smallest but generally more dense. The flocs formed from the Young Sound sediment in NaCl-supplemented tap water, however, are the least dense. The results from the present study fall well within the same area when plotted together with regressions of previous findings, of which the majority are in-situ investigations (Fig. 9). A plot of settling velocity versus mean floc size for all treatments is shown in Fig. 10 together with regression lines from some of the studies shown in Fig. 9 and two other studies. Fennessy et al. (1994) does not provide a regression equation on their settling velocity data (Fig. 6 in their paper) but the present data show a relationship quite similar to their data and the study by Mikkelsen and Pejrup (2001). The remaining studies found somewhat higher settling velocities in relation to floc size.
4. Discussion The present investigation demonstrates that flocculation efficiency is significantly higher in natural seawater than in filtered seawater with no or very little organic content, pointing to the influence of particulate organic matter on the settling of fine-grained minerogenic sediment. The effect was observed despite the low organic content of around 3% of the sediment. The flocs formed in unfiltered seawater showed a mean ESD of 117 μm as maximum, but flocs of more than 150 μm were observed during the experiments. The flocs in unfiltered seawater also exhibited the highest settling velocities of 0.33 ± 0.04 mm s-1, but were in general less dense than the flocs formed in the other treatments,
Fig. 3. Mean floc equivalent spherical diameter (ESD) for all three treatments with Sermilik sediment. 4
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 4. Volume concentrations (VC) for all three treatments with Sermilik sediment.
likely fundamental differences in the aggregation dynamics between high- and low-turbidity environments. These differences are likely also responsible for some of the scattering of the regression lines shown in Figs. 9 and 10. By filtration with the Whatman GF/F glass fibre filters with a 0.7 μm retention diameter the water is depleted of all POM, and the experiments showed that flocculation efficiency had visibly decreased compared to the experiments with unfiltered seawater. The flocs now showed a peak mean ESD of 97 μm with observed maximum sizes of about 110 μm. Ws was significantly lower even though the mean effective density generally was higher with an average 65 kg m−3. This highlights the importance of floc size on settling velocity, but it also suggests that the composition of the flocs were different. The result indicates that the presence of POM increases the porosity and thereby water content of the flocs, but electron microscopy images are necessary to determine the structure in more detail. In-situ investigations during diatom blooms have revealed macroflocs of several millimeters
natural suspensions with organic materials and biological processes is large. For example, fecal pellets produced by copepods, mussels and fish will be a significant contribution to the suspended load in many environments but they obviously do not flocculate into aggregates with similar characteristics. The aggregates found in suspension may also be formed at the bed as indicated by Forsberg et al. (2018) who showed how aggregation at the bed produced aggregates which are likely to constitute a substantial part of the “microfloc” population observed in many studies. It is not likely that the subsequent flocculation of microflocs in the water column into macro-flocs will produce flocs with similar characteristics and fractal dimensions as those formed at the sediment bed. However, fractal dimension may be a meaningful concept in some cases, for example when dealing with flocculation in highturbidity settings (e.g. Winterwerp et al., 2006) where flocculation in the water column will be dominating the aggregation processes. This is in contrast to low-turbidity settings where bioaggregates and biologically induced flocculation is likely to dominate and there is therefore
Fig. 5. Settling velocities measured for all three treatments with Sermilik sediment. The black line indicates the calculated settling velocity, Ws calc. (settling distance/settling time). 5
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 6. Comparison of mean floc equivalent spherical diameter (ESD) from Sermilik and Young Sound sediment treated with NaCl-supplemented tap water.
was observed in the particle ESD as well as in the VC (Figs. 3 and 4). This suggests a more rapid sedimentation of the entire sediment pool in the presence of DOM, which can contribute to large spatial and seasonal differences in sediment distribution and sedimentation patterns due to varying contents of DOM. The experiments with sediments from two fjord sites with different texture, minerogenic composition and OM content revealed significant variations in flocculation efficiency. The flocs formed from Young Sound sediment in NaCl-supplemented tap water was similar to flocs formed from the Sermilik sediment in filtered seawater regarding mean floc ESD, but the sedimentation rate was lower indicating a lower effective density (average of 33 kg m−3) of the flocs. However, the sedimentation rate of the Young Sound sediment was higher than the Sermilik sediment in NaCl-supplemented tap water, with significantly larger flocs. The exact reason for this difference is not known, but is likely caused by the slightly coarser primary particle distribution and the larger OM content of the sediment from Young Sound. Mineral composition may also play a role and this will be the subject of future
(Kranck and Milligan, 1988) and increases in settling velocity of two orders of magnitude (Alldredge and Gotschalk, 1989). Those flocs, however, were formed under low levels of shearing and with high levels of chl a (i.e. high concentrations of phytoplankton), which contrast with the conditions of the present investigation. Visible difference in flocculation extent was nonetheless found in this study, which illustrates the potential difference in distribution patterns of fine-grained sediment in seasonal transition periods, with less horizontal transport and more rapid sedimentation induced by POM. The presence of algae amplifies the flocculation processes, but dissolved substances alone have also been shown to enhance the process (e.g. De La Rocha et al., 2008; Markussen et al., 2016). The majority of the carbon pool in many aquatic environments is in dissolved form and may originate from for example microbial activity (e.g. reminiscences from an algae bloom) or from terrestrial washout (Thurman, 1985). The effect of DOM is shown by comparison of the flocs formed in filtered seawater to the flocs formed in NaCl-supplemented tap water. The two treatments exhibited similar settling velocities, but a clear difference
Fig. 7. Comparison of settling velocities (Ws) from Sermilik and Young Sound sediment treated with NaCl-supplemented tap water. The black line indicates the calculated settling velocity, Ws calc. (settling distance/settling time). 6
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 8. Comparison of volume concentrations (VC) from Sermilik and Young Sound sediment treated with NaCl-supplemented tap water.
studies. Mietta et al. (2009) observed an increase in floc sizes directly linked to the OM in the sediment, but similarly to the present study, the composition of the OM was not further investigated. The present investigation relies on laboratory experiments, but the materials used are all sampled in natural environments, and the findings can therefore be expected to be within the range of what can be observed in nature. However, some modifications were necessary in order to complete the experiments. Most importantly, the seawater samples were left in darkness for 24 h in order to obtain room temperature. When phytoplankton is exposed to complete darkness for a longer period, the cells will compensate by increased production of chl a and decreased growth (Jakobsen et al., 2012). Growth limitation is furthermore associated with an increase in the secretion of EPS (Thornton, 2002), which can play a dominant role in flocculation of particles (Droppo, 2001). However, the measured levels of chl a corresponded well to in-situ observations at the sampling site (NOVANA, 2017), which also showed that the sampling took place following a period of increased chl a levels indicating a phytoplankton bloom. Despite the low levels of chl a and POM, a clear difference was found between experiments with unfiltered and filtered seawater, which is
attributed to the presence of phytoplankton, even in very low concentrations. Even though the biological and chemical characteristics of the seawater might have been altered through the procedure used in the present investigation, the PCam system and the designated settling chamber offer a unique possibility to investigate isolated effects of different parameters of the flocculation process in high detail and under natural-like conditions in the laboratory or in-situ. Future studies should include an in-depth investigation of the chemical and biological composition of the water in which the flocs are formed, especially concerning algal species and cell counts. Such studies would contribute with further quantitative knowledge regarding the distribution and sedimentation of fine-grained cohesive sediments. 5. Conclusions Through a number of experiments, a particle camera system (PCam) was used to quantify the effects of particulate and dissolved substances present in low-turbidity natural seawater on flocculation of fine-grained cohesive sediment. Flocs formed in unfiltered seawater were Fig. 9. The calculated effective density as a function of mean floc equivalent spherical diameter (ESD). Blue dots: unfiltered seawater, green dots: filtered seawater, red dots: control, crosses: Young Sound sediment. The lines show results from previous investigations (Al Ani et al., 1991; Fennessy et al., 1994; Manning and Dyer, 1999; Mikkelsen and Pejrup, 2001; Markussen and Andersen, 2013). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
7
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Fig. 10. The settling velocity as a function of floc size. Blue dots: unfiltered seawater, green dots: filtered seawater, red dots: control, crosses: Young Sound sediment. The lines show results from previous investigations (Gibbs, 1985; Manning and Dyer, 1999; Mikkelsen and Pejrup, 2001; Agrawal and Pottsmith, 2000). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
significantly (p < 0.05) larger than flocs formed in NaCl-supplemented tap water. The settling velocities were similarly higher and the sedimentation of the total sediment volume was much more rapid. Through approximations by chlorophyll a levels and particulate organic matter (POM) content it is concluded that the concentration of algae in the seawater was low at the time of sampling, but both floc size and settling velocity was nevertheless increased in the presence of the algae. It was also shown that flocculation of particles was enhanced in seawater even when plankton (phyto- and zoo-) was removed compared to control experiments with NaCl-supplemented tap water. This suggests a tangible effect on the process induced by bacteria, dissolved orga nic matter, and/or chemical compounds. The present study further shows that sediment characteristics are of importance concerning the flocculation potential. More organic-rich and slightly coarser sediment formed larger, but less dense flocs than sediment with lower organic matter content.
Oceans 120, 5648–5667. Forsberg, P.L., Skinnebach, K.H., Becker, M., Kroon, A., Andersen, T.J., 2018. The influence of aggregation on cohesive sediment erosion and settling. Cont. Shelf Res. 171, 52–62. Gibbs, R.J., 1985. Estuarine flocs: their size, settling velocity and density. J. Geophys. Res. 90, 3249–3251. Hamm, C.E., 2002. Interactive aggregation and sedimentation of diatoms and clay-sized lithogenic material. Limnol. Oceanogr. 47, 1790–1795. Iversen, M.H., Ploug, H., 2010. Ballast minerals and the sinking carbon flux in the ocean: carbon-specific respiration rates and sinking velocity of marine snow aggregates. Biogeosciences 7 (9), 2613–2624. Jakobsen, R., Hansen, P.J., Daugbjerg, N., Andersen, N.G., 2012. The fish-killing dictyochophyte Pseudochattonella farcimen: adaptations leading to bloom formation during early spring in Scandinavian waters. Harmful Algae 18, 84–95. Keyvani, A., Strom, K., 2014. Influence of cycles of high and low turbulent shear on the growth rate and equilibrium size of mud flocs. Mar. Geol. 354, 1–14. Kiørboe, T., Hansen, J.L.S., 1993. Phytoplankton aggregate formation: observations of patterns and mechanisms of cell sticking and the significance of exopolymeric particles. J. Plankton Res. 15, 993–1018. Protocols for the joint global ocean flux study (JGOFS) core measurements. JGOFS Report Nr. vol. 19, vi+170 pp In: Knap, A., Michaels, A., Close, A., Ducklow, H., Dickson, A. (Eds.), Reprint of the IOC Manuals and Guides No. 29. UNESCO 1994. Kranck, K., Milligan, T., 1988. Macroflocs from diatoms: in situ photography of particles in bedford basin, nova scotia. Mar. Ecol. Prog. Ser. 44, 183–189. Lee, B.J., Toorman, E., Fettweis, M., 2014. Multimodal particle size distributions of finegrained sediments: mathematical modeling and field investigation. Ocean Dyn. 64, 429–441. Logan, B.E., 1999. Environmental Transport Processes. John Wiley & Sons, Hoboken, N. J., pp. 654. Manning, A.J., Dyer, K.R., 1999. A laboratory examination of floc characteristics with regard to turbulent shearing. Mar. Geol. 160, 147–170. Markussen, T.N., Andersen, T.J., 2013. A simple method for calculating in situ floc settling velocities based on effective density functions. Mar. Geol. 344, 10–18. Markussen, T.N., Elberling, B., Winter, C., Andersen, T.J., 2016. Flocculated meltwater particles control Arctic land-sea fluxes of labile iron. Sci. Rep. 6, 24033. Markussen, T.N., 2016. Parchar – characterization of suspended particles through image processing in Matlab. J. Open Res. Softw. 4 (1), e26. Mehta, A.J., 2014. An Introduction to Hydraulics of Fine Sediment Transport. Advanced Series on Ocean Engineering, vol. 38 World Scientific Publishing Co, Hackensack, NJ. Mietta, F., Chassange, C., Manning, A.J., Winterwerp, J.C., 2009. Influence of shear rate, organic matter content, pH and salinity on mud flocculation. Ocean Dyn. 59, 751–763. Mikkelsen, O.A., Pejrup, M., 2000. In situ particle size spectra and density of particle aggregates in a dredging plume. Mar. Geol. 170, 443–459. Mikkelsen, O.A., Pejrup, M., 2001. The use of a LISST-100 laser particle sizer for in-situ estimates of floc size, density and settling velocity. Geo Mar. Lett. 20, 187–195. Milligan, T., 1995. An examination of the settling behavior of a flocculated suspension. Neth. J. Sea Res. 33, 163–171. NOVANA, 2017. Det Nationale Program for Overvågning Af Vandmiljøet Og Naturen. WWW Page. http://havudsigten.dk/en/ensemble/oresund last visited on 28/02-19. Parsons, T.R., Maita, Y., Lalli, C.M., 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon, pp. 173. Passow, U., 2002. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55, 287–333. Passow, U., De La Rocha, C.L., 2006. Accumulation of mineral ballast on organic aggregates. Glob. Biogeochem. Cycles 20 (1), GB1013. Strom, K., Keyvani, A., 2016. Flocculation in a decaying shear field and its implications
Acknowledgement The authors would like to thank Thor Nygaard Markussen for constructive discussions, development and modification of the Matlab script. Comments and suggestions by two anomous reviewers were also greatly appreciated. This work was supported by the Velux Foundations, grant nos. 17668 and 18533. References Agrawal, Y.C., Pottsmith, H.C., 2000. Instruments for particle size and settling velocity observations in sediment transport. Mar. Geol. 168, 89–114. Al Ani, S., Dyer, K.R., Huntley, D.A., 1991. Measurement of the influence of salinity on floc density and strength. Geo Mar. Lett. 11, 154–158. Alldredge, A.L., Gotschalk, C.C., 1989. Direct observation of the mass flocculation of diatom blooms – characteristics, settling velocity and formation of diatom aggregates. Deep-Sea Res. Part A: Oceanograph. Res. Papers 36 (2), 159–171. Avnimelech, Y., Troeger, B.W., Reed, L.W., 1982. Mutual flocculation of algae and clay: evidence and implications. Science 216, 63–65. De La Rocha, C.L., Nowald, N., Passow, U., 2008. Interactions between diatom aggregates, minerals, particulate organic carbon, and dissolved organic matter: further implications for the ballast hypothesis. Glob. Biogeochem. Cycles 22 (4), GB4005. Droppo, I.G., 2001. Rethinking what constitutes suspended sediment. Hydrol. Process. 15 (9), 1551–1564. Eisma, D., Bernard, P., Cadee, G., Ittekkot, V., Kalf, J., Laane, R., Martin, J., Mook, W., van Put, A., Schuhmacher, T., 1991. Suspended-matter particle size in some WestEuropean estuaries; Part II: a review on floc formation and break-up. Neth. J. Sea Res. 28 (3), 215–220. Fennessy, M.J., Dyer, K.R., Huntley, D.A., 1994. INSSEV: an instrument to measure the size and settling velocity of flocs in situ. Mar. Geol. 117, 107–117. Fettweis, M., Baeye, M., 2015. Seasonal variation in concentration, size, and settling velocity of muddy marine flocs in the benthic boundary layer. J. Geophys. Res.:
8
Estuarine, Coastal and Shelf Science 228 (2019) 106395
K.H. Skinnebach, et al.
Verspagen, J.M.H., Visser, P.M., Huisman, J., 2006. Aggregation with clay causes sedimentation of the buoyant cyanobateria Mycrocystis spp. Aquat. Microb. Ecol. 44, 154–174. Winter, C., Becker, M., Ernstsen, V.B., Hebbeln, D., Port, A., Bartholoma, A., Lunau, M., 2007. In-situ observation of aggregate dynamics in a tidal channel using acoustics, laser diffraction and optics. J. Coast. Res. SI 50, 1173–1177. Winterwerp, J.C., 2002. On the flocculation and settling velocity of estuarine mud. Cont. Shelf Res. 22 (9), 1339–1360. Winterwerp, J.C., Manning, A.J., Martens, C., de Mulder, T., Vanlede, J., 2006. A heuristic formula for turbulence-induced flocculation of cohesive sediment. Estuar. Coast Shelf Sci. 68, 195–207. Wolanski, E., 2007. Estuarine Ecohydrology, Chapter 3. Elsevier, Amsterdam, The Netherlands. Zhang, N., Thompson, C.E.L., Townend, I.H., Rankin, K.E., Paterson, D.M., Manning, A.J., 2018. Nondestructive 3D imaging and quantification of hydrated biofilm-sediment aggregates using X-ray microcomputed tomography. Environ. Sci. Technol. 52, 13306–13313. https://doi.org/10.1021/acs.est.8b03997.
for mud removal in near-field river mouth discharges. J. Geophys. Res.: Oceans 121, 2142–2162. Thornton, D.C.O., 2002. Diatom aggregation in the sea: mechanisms and ecological implications. Eur. J. Phycol. 37 (2), 149–161. Thurman, E.M., 1985. Organic Geochemistry of Natural Waters. Kluwer Academic, pp. 497. Tolhurst, T.J., Gust, G., Paterson, D.M., 2002. The influence on an extra-cellular polymeric substance (EPS) on cohesive sediment stability. In: Winterwerp, J.C., Kranenburg, C. (Eds.), Fine Sediment Dynamics in the Marine Environment – Proceedings in Marine Science 5. Elsevier, Amsterdam, pp. 409–425. Turner, A., Millward, G.E., 2002. Suspended particles: their role in estuarine biogeochemical cycles. Estuar. Coast Shelf Sci. 55 (6), 857–883. Underwood, G.J.C., Kromkamp, J., 1999. Primary production by phytoplankton and microphytobenthos in estuaries. Adv. Ecol. Res. 29, 93–153. Underwood, G.J.C., Paterson, D.M., 2003. The Importance of Extracellular Carbohydrate Production by Marine Epipelic Diatoms. Advances in Botanical Research (Incorporating Advances in Plant Pathology), vol. 40. Elsevier, Amsterdam, pp. 183–240.
9