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Pandey 2018
Pandey 2018
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
Original Articles
A R T I C L E I N F O A B S T R A C T
Keywords: In the present study, the ecological status of four major South Korean rivers flowing near industrial complexes is
Biomonitoring assessed using physico-chemical analyses and various descriptors based on benthic diatom assemblages.
Diatoms Principal component analysis conducted with physical and chemical variables singled-out four sites as more
Lipid bodies severely impacted (higher concentration of metals and total nitrogen, higher conductivity and biological oxygen
Deformities
demand), while the remaining 12 sites indicated less impacted conditions, although showing nutrient enrich-
Diatom assemblages
ment. Less-contaminated sites based on physico-chemical properties showed higher cell densities, higher rich-
Diversity
Cell size ness and diversity, a larger proportion of live and healthy-looking diatoms, lower production of lipid bodies (in
terms of number and size) and fewer teratologies than more-contaminated sites. Non-taxonomical metrics (cell
heath status, cell size, lipid bodies and valve deformities) were in good agreement with traditional taxonomical
metrics (assemblage structure, richness, diversity). Overall, water quality assessment based on diatom assem-
blages and diatom-based metrics had a good fit with the available physico-chemical data and agreed on the most
impacted sites. However, additional sites showed signs of degradation based on the diatom metrics used. This
suggests that the use of biotic indicators provides useful complementary information on the health status at the
selected sites.
⁎
Corresponding author at: Department of Marine Science, Incheon National University, 119, Academy-ro, Yeonsu-gu, Incheon 22012, Republic of Korea.
E-mail address: [email protected] (T. Han).
http://dx.doi.org/10.1016/j.ecolind.2017.07.043
Received 21 March 2017; Received in revised form 19 July 2017; Accepted 21 July 2017
Available online 25 September 2017
1470-160X/ © 2017 Elsevier Ltd. All rights reserved.
L.K. Pandey et al. Ecological Indicators 84 (2018) 140–151
Fig. 1. Study area showing the 16 sites selected on four main Korean rivers.
to environmental fluctuations as compared with higher-level organ- used in the development of diatom-based indices (Kelly and Whitton,
isms. In particular, diatoms (Bacillariophyta) have been extensively 1995; Ponader et al., 2007; Coste et al., 2009; Lavoie et al., 2006,
included in water quality assessment for monitoring the biological in- 2014). Multi-metric diatom indices have already been developed
tegrity of lotic ecosystems under various stresses such as eutrophica- (Zalack et al., 2010), but generally include taxonomy-derived metrics
tion, salinization, as well as metal and organic contamination (Gold such as % tolerant species, richness and chlorophyll a (Fore and Grafe,
et al., 2002; Debenest et al., 2008; Lavoie et al., 2014). Diatoms are a 2002). Various non-taxonomic diatom descriptors such as cell health
group of algae exhibiting a large diversity in terms of taxonomy, mor- status, motility, lipid bodies, cell density and teratologies (abnormal
phology and ecology, and are present in most aquatic and humid en- valves) are well documented as biomonitoring tools. For example,
vironments (Round et al., 1990). Diatoms have specific degrees of tol- Morin et al. (2012) reviewed the response of diatoms to metal con-
erance to environmental variables and have a rapid reproduction rate, tamination from the individual level (e.g., size, growth form, and
which are among the characteristics making them excellent indicators morphological abnormalities) to the assemblage structure level (turn-
of aquatic biological integrity (Kelly et al., 2008; Stevenson et al., 2008, over from sensitive to tolerant species). Similarly, Pandey and Bergey
2010). Subtle changes in environmental conditions may cause a shift in (2016) used various metrics to monitor the effect of chronic metal ex-
assemblage structure; sensitive diatoms decrease in abundance, while posure (Cu and Zn) on benthic diatoms, and reported a reduction in
tolerant species increase (Van Dam et al., 1994; Harding et al., 2005). diatom motility and cell size, as well as an increase in lipid body con-
The analysis of the diatom assemblage structure and species’ autecology tent and in teratology frequency.
allows for the characterization of past and present environmental In this study, benthic diatom assemblages from 16 sites selected
conditions and health status in a system (Kelly et al., 2008; Leira et al., along four major South Korean rivers flowing in close proximity to
2015; Schallenber and Saulnier-Tablbot, 2015). Diatom-based mon- industrial complexes and municipal effluents were examined to eval-
itoring is also gaining in popularity for the assessment of ecosystem uate their ecological status. For this purpose, multiple biological de-
rehabilitation to evaluate recovery success (e.g., Coe et al., 2009; Feld scriptors were used. First, more traditional metrics based on diatom
et al., 2011; Arini et al., 2012; Hamilton et al., 2015; Żelazna-Wieczorek assemblage composition, richness, diversity and cell density were ex-
and Nowicka-Krawczyk, 2015). amined. Additional biological metrics were also investigated: cell size
To adequately estimate the biological status of a system before and distribution, diatom health status (live, unhealthy or dead), and the
after alteration or rehabilitation, it is fundamental to develop appro- presence of lipid bodies and teratologies. Finally, we compared the
priate biological metrics. An approach based on multiple descriptors information provided by the various diatom-based metrics examined
may provide a more complete and integrated picture of the environ- with the estimation of the water quality status of each site based on a
mental conditions experienced by the diatoms, as compared with the suite of physico-chemical characteristics.
more traditional taxonomic approach (assemblage structure) generally
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L.K. Pandey et al. Ecological Indicators 84 (2018) 140–151
On-site water quality measurements and surface water collection 2.4. Taxonomical analysis and assessment of teratologies
were performed in September 2015 at the 16 selected sites following
the guidelines of the National surveys for stream ecosystem health Clean diatom frustules were also examined after digesting cell
(MOE, Korea). Temperature, pH, and dissolved oxygen were measured content to facilitate taxonomical identification and to assess the pre-
directly in the field with a multi-parameter display system (YSI 650, sence of abnormal valves. The fresh material collected was first treated
USA). Conductivity was measured in the field with a portable meter with 90% acetone to remove cytoplasmic content. Subsequently, the
(Milwaukee, USA). Total dissolved solid measurements were performed samples were dried for 30 min at 25 °C and treated with concentrated
in the field with an amperometric graphite electrode (HI98301 DiST® H2SO4 (99.99%, analytical grade, Sigma-Aldrich, St. Louis, USA) fol-
1). Biochemical oxygen demand was measured by dark and light bottle lowed by hydrogen peroxide (30%) (w/w, analytical grade, Sigma-
incubation for 24 h at 20 °C in controlled light conditions. EPA-ap- Aldrich, St. Louis, USA). The cleaned samples were then washed 10
proved Colilert-18 test by IDEXX was carried out to estimate total co- times with deionized water to remove the acid present inside the cells
liforms. A water automatic analyzer (Skalar/Netherlands, SAN ++) and in the liquid fraction. Diluted samples were spread onto cover slips
was used to measure total nitrogen (TN) and total phosphorus (TP). for drying. Permanent slides were mounted in Pleurax mounting
Analyses of metals (As, Ag, Cd, Cr, Cu, Hg, Ni, Pb and Zn) were con- medium (refractive index = 1.73) for microscopic examination.
ducted by inductively coupled plasma-optical emission spectro- Diatoms were counted and identified using images from Algaebase
photometer (ICP-OES; Varian Vista PRO, CA, USA) using 15 ml water (Academy of Natural Sciences of Philadelphia, http://diatom.acnatsci.
samples. Standard solutions were prepared fresh and calibration curves org/AlgaeImage/) and the Algal image database of India (AIDI)
(r2 > 0.995) were performed. To ensure the quality of the measure- (Pandey et al., 2016). Monographs on diatoms by Patrick and Reimer
ments, standard solutions were analyzed after every 10 samples to (1966, 1975) and a manual on stream periphyton by Biggs and Kilroy
verify their concentrations. Measurement precision ranged from 94 to (2000) were also consulted. A total of 500 valves per sample were
107%, and detection limits were calculated based on the standard de- enumerated. Diatom assemblage composition was expressed as percent
viations of blanks triplicates (range: 4–14 μg L−1). Organic compounds relative abundance. Qualitative and quantitative assessments of valve
were analyzed by the South Korean Ministry of the Environment, fol- deformities were conducted using permanent diatom slides (n = 3).
lowing the methods presented in Cho et al. (2014). All samples col- Deformities in diatom frustules were categorized into five types: (1)
lected for analyses of metals and organic compounds were previously deformities in valve outline, (2) deformities in striations, (3) defor-
filtered through 0.45 μm filters. mities in the sternum/raphe structure, (4) mixed deformities and (5)
deformities in the costae (Falasco et al., 2009a; Pandey et al., 2014,
2.3. Benthic diatom sampling and fresh material analyses 2015). Diatom cell biovolumes were classified in three categories based
on Omnidia database (https://hydrobio-dce.irstea.fr/telecharger/
Benthic diatom assemblages were collected in September 2015 from diatomees-ibd/): small (< 400 μm3), intermediate (400–4000 μm3),
hard surfaces (concrete walls, scrapped surface area ∼25 cm2) using a and large (> 4000 μm3).
new toothbrush at each of the 16 selected sites. Six samples from each
site were collected and pooled together to obtain a composite sample 2.5. Statistical analyses
(Winter and Duthie, 2000; Lavoie et al., 2006). The collected material
was placed in a plastic bottle with 5 ml of river water, kept cold and Shannon’s diversity index values were calculated using the freeware
transported to the laboratory, and analyzed within one week. Fresh “PAST” (Hammer et al., 2001) for each pseudo-replicate (n = 3). A
samples were analyzed under a light microscope at 450× and 100× preliminary detrended correspondence analysis was conducted on
magnification (Zeiss, Axioskop 2, equipped with a Nikon camera) for species data and revealed a short gradient length (1.06) suggesting a
live diatom observation. All diatom cells were counted to estimate linear response. Principal component analyses (PCAs; Euclidian dis-
densities with a Spencer’s haemocytometer at 450× magnification tance) were thus conducted to explore site distribution based on (i)
using three aliquots of 1 ml (pseudo-replicates, n = 3) of composite physico-chemical variables and (ii) diatom species assemblages. En-
biofilm sample. Fresh diatom cells were examined to evaluate health vironmental data were centered and standardized. Diatom relative
status (live, unhealthy and dead cells), and for the presence of lipid species abundances were square root transformed. Only the species
bodies (LBs). Diatom cells were categorized as live or healthy (with present at a relative abundance of ≥1% (in at least one sample) were
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Table 1
Physical and chemical variables measured in the surface water of the 16 sites. nd = under detection limit.
River Site DO mg BOD5 mg Coli CFU Temp °C Cond pH TN mg TP mg TDS mg Cu mg Ni mg l−1 Zn mg l−1
l−1 l−1 ml−1 μS cm−1 l−1 l−1 l−1 l−1
Nakdong Ayang 11.44 1.51 2 23.4 470 8.8 5.96 0.028 380 nd nd 0.075
Dalseo 11.54 1.93 10 27.3 2895 7.67 10.04 0.084 1704 0.029 0.068 0.017
Keumho 11.55 2.08 9 26.4 2580 8.16 10.93 0.112 2180 0.048 0.045 0.034
Yeongsan Gwangjugong 11.1 2.08 72 22.1 309 8.02 3.96 0.111 184 nd nd 0.071
Gwangju-1 11.65 1.43 6 23.4 204 9.25 2.23 0.013 190 nd nd 0.071
GJ-2 11.75 1.49 5 22.8 321 7.87 3.91 0.111 242 nd nd 0.05
PD-1 11.77 1.66 19 20.6 170 7.67 5.51 0.115 276 nd nd 0.07
Geum Ohryang 11.75 0.71 16 23.4 439 7.6 6.22 0.34 282 nd nd 0.09
Bangchuk 11.12 2.53 8 23.2 438 8.14 16.04 0.194 40 nd nd 0.062
Masan 11.3 3.14 15 23.3 321 8.38 7.23 0.297 302 nd nd 0.057
Sucheol 11.48 1.44 5 22.4 362 8.74 7.14 0.304 302 nd nd 0.053
Miho-5 11.45 2.63 15 21.5 659 7.45 7 0.12 454 nd nd 0.081
Miho-8 11.44 1.22 4 24.0 482 8.15 3.83 0.12 268 nd nd 0.079
Miho-7 11.33 1.25 46 21.8 505 7.72 5.44 0.111 342 0.004 nd 0.075
Han Soyo 10.34 9.25 240 27.6 4007 7.72 14.19 0.098 2132 nd 0.021 0.3
Daejeon 10.86 3.43 64 24.7 2579 8.35 9.88 0.097 898 0.043 0.016 0.44
included in the PCA. Ordinations were performed with the software sampling of September 2015. A PCA was conducted to explore site dis-
CANOCO 5.0 (ter Braak and Šmilauer, 2012). tribution based on surface water characteristics (Fig. 2), and showed distinct
differences among sampling sites. The PCA biplot explained 69% of the
3. Results and discussion variance (PCA axis 1 contributed 50% and PCA axis 2, 19%). The ordination
indicates that Dalseo, Keumho, Soyo and Daejeon cluster on the right-hand
3.1. Environmental characteristics of the study sites side of the biplot. Within the 16 sites, these four sites have higher con-
centrations of Ni/Cu or Zn and nutrients (TN), along with high conductivity,
Values of the chemical and physical variables measured at the 16 sites TDS, BOD5, and coliforms, and were therefore classified as “severely im-
are presented in Table 1. Three metals detected in water samples were pacted”. The 12 other sites occupy the left-hand side of the biplot and
above quantification limits with elevated values: Cu (Keumho - cluster close to the center. These sites generally have high nutrient con-
= 0.048 mg l−1), Zn (Daejeon = 0.44 mg l−1), Ni (Dalseo - centrations potentially reflecting eutrophication, but were classified here as
−1
= 0.068 mg l ). Certain sites showed elevated conductivity values (Soyo, “less-impacted” because chemical analyses did not reveal any metal con-
Dalseo, Keumho, Daejeon > 2000 μS cm−1) and coliforms tamination. Dalseo, Keumho, Soyo and Daejeon cluster apart from the other
(Soyo = 240 CFU ml−1). The data also reflected nutrient enrichment at sites mostly due to high metal concentrations at these sites (values were
most sites with mean TP reaching 0.141 mg l−1 (ran- under detection limits at the other sites). However, a PCA conducted
ge = 0.013–0.34 mg l−1) and mean TN reaching 7.5 mg l−1 (ran- without metal data (results not presented) also revealed that these four sites
ge = 2.23–16.04 mg l−1). Although governmental routine monitoring fre- stood apart from the others, principally along a gradient of total nitrogen,
quently reports the presence of organic contaminants (Cho et al., 2014), coliforms, BOD5, and conductivity. In general, based on the available water
concentrations were found to be under detection limit based on the water quality parameters, the sampling sites on the Nakdong and Han rivers
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Fig. 5. Species richness and Shannon diversity index values (Mean ± SE; n = 3) of
diatom assemblages collected at the 16 sites.
Fig. 4. Diatom cell density (Mean ± SE; n = 3) in samples collected at the 16 sites.
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L.K. Pandey et al. Ecological Indicators 84 (2018) 140–151
Fig. 6. Diatom assemblages collected at the 16 sites sampled in four major South Korean rivers. Black, grey and white sections show the relative abundances of diatom size classes: small
(< 400 μm3), intermediate (400–4000 μm3), and large (> 4000 μm3).
3.3. Comparing PCAs: one-time water chemistry versus diatom assemblages separated the sites into two main groups that may be coarsely char-
acterized as “severely impacted” and “less-impacted”. However, the
Comparing site distribution based on physico-chemical variables diatom-based PCA suggests that, in addition to Dalseo, Keumho, Soyo
versus diatom assemblages revealed similarities in overall water quality and Daejeon, the assemblages from Ayang and GJ-2 may also reflect
assessment: Dalseo, Soyo and Daejeon clustered apart from the other impacted conditions. This situation may represent a good example in
sites in both approaches, suggesting more contaminated environments. which the biota provides additional information on water quality status
The diatom assemblage structure observed at GJ-2 was similar to the beyond traditional chemistry measurements. The fact that Ayang and
assemblages found at the three above-mentioned sites, which suggests GJ-2 suggest more impacted conditions based on diatom assemblages
that this site may also have impacted conditions. Keumho, classified as compared to chemistry-based assessment may result from temporally
severely impacted based on chemistry, also clustered apart from the fluctuating contamination (e.g., episodic releases). The timing of spot
sites showing less impacted conditions. Ayang may also be severely sampling for water chemistry analyses may not correspond to the re-
impacted as it clustered with Keumho and was apart from the other lease of pollutants, such as metals.
sites. Overall, the two PCAs conducted using chemistry or diatoms
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L.K. Pandey et al. Ecological Indicators 84 (2018) 140–151
Fig. 8. Gradient in lipid body biovolume observed in six commonly occurring diatom species (a) Navicula gregaria, (b) Navicula capitatoradiata, (c) Nitzschia inconspicua, (d) Navicula
rostellata, (e) Nitzschia frustulum and (f) Nitzschia palea. Scale bar = 7 μm.
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L.K. Pandey et al. Ecological Indicators 84 (2018) 140–151
Table 2a
Overall range in % biovolume contribution of lipid bodies to total cell biovolume at each site.
Sites Ayang Dalseo Keumho Gwangjugong Gwangju-1 GJ-2 PD-1 Ohryang Masan Sucheol Bangchuk Miho-5 Miho-8 Miho-7 Soyo Daejeon
% biovolume 4–7 8–28 5–40 2–5 4–7 2–6 1–3 2–5 2–7 1–5 4–7 2–6 4–7 2–6 5–60 12–55
contribution
of LBs to total
cell volume
Table 2b
Detailed lipid bodies status in six commonly occurring diatom species. Sites have been grouped as severely contaminated (Dalseo, Keumho, Soyo and Daejeon) and less-contaminated
waters bodies (other 12 sites) based on the chemistry-based ordination.
Number of lipid bodies Diameter (μm) of lipid bodies % biovolume contribution of lipid bodies to total cell volume
Less contaminated Contaminated sites Less contaminated Contaminated sites Less contaminated sites Contaminated sites
sites sites
index at acid mine drainage sites than at reclaimed sites, while Barral- which did not seem to reflect metallic contamination based on the
Fraga et al. (2016) reported lower values for these metrics in diatom- available data. On the other hand, the ordination conducted on diatom
dominated biofilms contaminated with arsenic. Similarly, the diatom assemblages (PCA) indicated severely impacted conditions for these
assemblages collected in the present study showed lower species rich- two sites (Fig. 3) that may not have been noticed based solely on the
ness (10–23) and/or Shannon’s diversity index (1.6–2.0) at polluted available chemistry data. It is also possible that factors other than
sites Ayang, Dalseo, Keumho, GJ-2, Soyo and Daejeon, but also at sites contamination favored small diatoms, including grazing and coloniza-
Gwangjugong and Gwangju-1. PD-1, Ohryang, Bangchuk, Masan, Su- tion phase following a physical disturbance. Gwangjugong, PD-1,
cheol, Miho-5, Miho-8 and Miho-7 showed higher species richness Masan, and Miho-5 showed high proportions of small-sized diatoms,
(30–50) and Shannon diversity index (2.6–3.8) (Fig. 5). As a general although neither of these sites was considered as severely impacted
trend, the sites clustered on the right-hand side of the PCA (Fig. 2) with based on chemistry or diatom assemblage data. This suggests that cell-
more severely degraded conditions were associated with lower richness size alone may not provide a complete picture of an ecosystem’s health
and diversity. However, these metrics also showed lower values for status. However, as a general trend, the sites that were considered less
certain sites that were not considered as severely impacted, based on contaminated showed a dominance of intermediate and large diatom
chemical analyses. This lack of concordance at some sites may suggest species, reaching up to more than 50% of the assemblage.
that the available one-time physico-chemical data do not reflect the
temporally fluctuating nature of these waters and that diatom diversity 3.4.4. Diatom cell health status
brings additional insight on the environmental integrity of the sites. It Investigation of live and dead diatoms in the assemblage may pro-
may also indicate that diversity and richness are not always good vide additional environmental information (Cox, 1998; Stevenson and
proxies of water quality, and perhaps should not be used alone as Pan, 1999; Gillett et al., 2011). Wood et al. (2014, 2016) reported
bioindicators. This aspect is discussed in Blanco et al. (2012), where health status of diatoms (intact vs. unhealthy cells) as a sensitive and
diversity indices are reported to generally exhibit poor linear correla- rapid method for assessing herbicide toxicity. Gillett et al. (2009) ar-
tions with environmental factors indicating ecological status. Further- gued that conventional diatom cell count methods provide taxonomical
more, sampling effort or sample size may strongly affect richness and confidence while the live diatom count offers better ecological relia-
diversity values, thus influencing water quality status comparisons. bility. In a general biomonitoring perspective, both approaches are
However, this does not represent an issue in the present study as the valuable and complementary. Among the 16 sites examined, Gwangju-
same protocol was used for all samples (∼500 frustules per sample). 1, PD-1, Ohryang, Bangchuk, Masan, Sucheol, Miho-5, Miho-7 and
Miho-8 showed a predominance (40–50%) of live frustules (Fig. 7),
3.4.3. Cell size while percent unhealthy frustules showed higher values (> 40%) at
It has been shown in numerous studies that small-sized species tend Dalseo and GJ-2. Percent dead frustules in the diatom assemblages
to dominate in metal-contaminated environments (Ivorra et al., 1999; showed higher values (40–65%) at Ayang, Gwangjugong, Soyo and
Morin et al., 2008, 2012; Tlili et al., 2011; Barral-Fraga et al., 2016). Daejeon. As a general trend, the less-impacted sites clustering on the
Decrease in diatom frustule size within a given species has also been left-hand side of the diatom-based ordination (Fig. 3) also showed
reported as a response to metal stress. For example, Cattaneo et al. higher proportions of live diatoms, suggesting healthier conditions. This
(2004) reported that metal contamination within sediment cores from a trend was not as clear when relating diatom health status and chemistry
Canadian lake was responsible for size reduction. Similarly, Luís et al. data, indicating that diatoms may have responded to other stresses or
(2011) reported size decline in Brachysira vitrea frustules at metal- that there is a time lag between water quality change and cell de-
contaminated sites of Corona stream, Portugal. In the present in- gradation. It is also possible that the presence of dead cells is in-
vestigation, the four sites considered as the most impacted based on dependent of site degradation. For example, very low water velocity
physico-chemical parameters (Dalseo, Soyo, Daejeon, Keumho) were may favor dead cell deposition. However, all sites sampled in this study
characterized by a dominance of small adnate diatom species (Fig. 6). were characterized by relatively low flow, which suggests that the
Ayang and GJ-2 also showed high abundances of small-sized diatoms, variation in diatom health status among sites are more likely to reflect
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L.K. Pandey et al. Ecological Indicators 84 (2018) 140–151
Fig. 9. Deformed frustules observed in various diatom species (a) Ulnaria ulna, (b) Cymbella turgidula, (c) Cocconeis placentula, (d) Gomphonema parvulum, (e) Achnanthes exigua, (f)
Eolimna minima, (g) Diatoma vulgaris, (h) Tabularia fasciculata, (i) Fragilaria capucina, (j) Staurosira construens and (k) Planothidium frequentissimum. “N” denotes normal frustules. Scale
bar = 5 μm.
water quality than differences in dead cell accumulation. to a metal stress, as LBs were observed with higher abundances and
larger sizes at the sites showing the highest concentrations of metals.
3.4.5. Lipid bodies However, it is important to note that other environmental stresses may
Lipid bodies constitute energy reserves in algae. Under stressed have influenced LB production and that this was not assessed in this
conditions (e.g. nutrient depletion, metal contamination, excess light), study. LB stimulation by metal contamination has been widely reported
these lipid droplets are reported to increase in number and size (Pandey (Einicker-Lamas et al., 2002; Liu et al., 2008; Wang et al., 2009; Pillai
et al., 2015; Yang et al., 2013; Liang et al., 2015; d’Ippolito et al., 2015). et al., 2014; Pandey et al., 2015, 2016; Gautam et al., 2017). LBs are
The number of LBs and their respective diameters were examined in six promising biomarkers of stress although more research is required to
commonly occurring diatom species at the 16 study sites (N. gregaria, N. define their variability under various natural conditions for optimal use
capitatoradiata, N. inconspicua, N. rostellata, N. frustulum and N. palea) in a bioassessment perspective. The approach is relatively easy, as
(Fig. 8). Table 2a presents the range in % biovolume contribution of taxonomical skills are not required (all diatom species are likely to
lipid bodies to total cell volume at each site, while Table 2b presents a produce LBs in larger number and size under stressed conditions).
detailed summary of the LB's characteristics for the six most common
species in which LBs were counted and measured. Looking at the sites 3.4.6. Deformities
individually, the proportion of LBs relative to cell biovolume was Numerous studies relate deformities with environmental dis-
higher for Soyo, Daejeon, Dalseo and Keumho (Table 2a). A marked turbances (see review in Falasco et al., 2009a), particularly in metal-
difference in LBs was observed when comparing contaminated sites contaminated conditions (Morin et al., 2012; Lavoie et al., 2012;
versus less-contaminated sites (based on physico-chemistry data) where Leguay et al., 2016; Pandey and Bergey, 2016). In the present study, 13
more impacted conditions seemed to have stimulated LB production. In species out of the total 65 species identified showed deformities in their
the present study, lipid body analysis suggests that diatoms responded frustules (Fig. 9). Deformed frustules were encountered in small
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Table 3
Summary of the water quality descriptors used in this study and site classification as “severely impacted (grey)” or “less-impacted (white)”
based on each metric.
straightforward because fewer metrics suggested degraded conditions at Appendix A. Supplementary data
these sites. The fact that some diatom metrics are more likely to respond
quickly to changes in chemistry, in contrast to more resilient indicators Supplementary data associated with this article can be found, in the
such as taxonomical composition, may reflect progressive recovery/de- online version, at http://dx.doi.org/10.1016/j.ecolind.2017.07.043.
gradation of sites. This explanation could be of particular interest at
Gwangjugong, where rehabilitation operations have been undertaken. References
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