Environ Monit Assess (2020) 192: 626

https://doi.org/10.1007/s10661-020-08582-x

Assessment of benthic macroinvertebrate response

to anthropogenic and natural disturbances
in the Kodungallur-Azhikode estuary, southwest coast
of India
P. R. Jayachandran & M. Jima & J. Philomina &
S. Bijoy Nandan

Received: 9 October 2019 / Accepted: 27 August 2020 / Published online: 8 September 2020
# Springer Nature Switzerland AG 2020

Abstract Benthic biotic indices are important ecologi- AMBI, ‘high to moderate’ condition in BENTIX, ‘high
cal tools extensively used to understand the ecological to poor’ condition in BOPA and ‘moderate to poor’
quality of coastal wetlands. The present study aimed to condition in univariate Shannon diversity index. All
assess the ecological status of Kodungallur-Azhikode the multivariate indices tested in the study were corre-
estuary for the first time by using widely used benthic lated with each other except BOPA and M-AMBI. The
indices such as species richness (S), Shannon diversity group of stations dominated with a sandy substrate and a
index (H′log2), BENTIX, benthic opportunistic poly- moderate level of organic content indicated high to good
chaetes amphipods (BOPA), AZTI’s Marine Biotic In- conditions while other stations demonstrated moderate
dex (AMBI) and multivariate AMBI (M-AMBI). In the to poor conditions. However, no significant variation in
canonical correspondence analysis, salinity, dissolved indices tested between seasons was observed. The pres-
oxygen, organic matter, sediment Eh, sediment pH and ent study recommends long-term monitoring of benthic
sand were identified as important variance descriptors. macroinvertebrate assemblages with proper taxonomic
A single species of an opportunist, Americorophium identification and functional trait analysis for better
triaeonyx, an amphipod belonging to the ecological calibration of indices, which is the key factor for getting
group (EG) III, significantly contributed to the total better results.
macrofaunal density. Other dominant opportunistic spe-
cies included Obelia bidentata (EGII), Arcuatula Keywords Wetlands . Ecological health . Marine biotic
senhousia (EGIII), Cirolana fluviatilis (EGII), indices . Cochin backwater . Marine pollution .
Prionospio cirrifera (EGIV) and Capitella sp. (EGV). Vembanad Lake
The overall assessment indicated a ‘good to moderate’
condition in AMBI, ‘good to poor’ condition in M-
Introduction
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s10661-020-08582-x) contains
supplementary material, which is available to authorized users.
Biotic indices based on macroinvertebrates are broadly
accepted by the scientific community worldwide for
P. R. Jayachandran (*) : M. Jima : J. Philomina : assessing the ecological state of coastal marine ecosys-
S. Bijoy Nandan (*) tems (Borja et al. 2000). Macroinvertebrates have a
Department of Marine Biology, Microbiology and Biochemistry, sessile or sedentary life habit and a relatively long
School of Marine Sciences, Cochin University of Science and
Technology, Lakeside Campus, Fine Arts Avenue, Kochi, Kerala lifespan and are exposed to various ecosystem variations
682016, India in the overlying water masses (Blanchet et al. 2008;
e-mail: [email protected] Dauer 1993; Jayachandran et al. 2012; McLusky and
e-mail: [email protected] Elliott 2004). Several studies have also revealed their
626 Page 2 of 19 Environ Monit Assess (2020) 192: 626

sudden response to anthropogenic and natural distur- abundance, species number, composition, diversity,
bances (Asha et al. 2016; Bijoy Nandan 2008; richness, dominance and evenness) and (iii) to examine
Blanchet et al. 2008; Equbal et al. 2018; Jayachandran the effectiveness and/or limitations in assessing the eco-
and Bijoy Nandan 2012; Kennish 2002; Kennish and logical condition of tropical monsoonal estuaries.
Townsend 2007; Pearson and Rosenberg 1978). They
are an extremely diverse group with a variety of life-
styles and tolerance level from the ecosystem distur- Materials and methods
bances, allowing their classification into different eco-
logical functional groups (Jayachandran et al. 2019b; Study area
Pearson and Rosenberg 1978). They have a fundamental
role in the ecosystem by providing links to the higher The Kodungallur-Azhikode estuary (KAE) is a part of
trophic levels (Abdul Jaleel 2012; Damodaran 1973; the Vembanad Kol wetland ecosystem, which is one of
McLusky and Elliott 2004; Vineetha et al. 2020). These the Ramsar sites in the Kerala state of India (Bijoy
organisms play a significant role in chemical fluxes Nandan 2008; Don Xavier et al. 2019). The estuary is
between the sediment-water interface through bioturba- considered as a monsoonal microtidal estuary
tion and suspension-feeding activities (Reiss and characterised by the mixed semidiurnal tides. The coast-
Kröncke 2005). Therefore, the use of macroinverte- al region of the study stations (10°–10° 20′ N and 76°
brates as bioindicators possesses certain advantages 10′–76° 20′ E) has an area of 300 km2 with a high
over other communities (Ajmalkhan et al. 2004; average population density (1850 persons per km2).
Jayachandran et al. 2019a; Jayachandran et al. 2019c; The heavy river discharge during the south-west mon-
Jayachandran et al. 2018a; Jayachandran et al. 2018b; soon season creates a riverine condition in the estuary
Jayachandran et al. 2015; Oliver et al. 2018a; Oliver (Revichandran 1993; Revichandran and Abraham 1998;
et al. 2018b; Philomina et al. 2019; Philomina et al. Revichandran et al. 2012; Vijith et al. 2009). In recent
2018; Rahayu et al. 2020). For these reasons, years, the KAE has undergone deterioration mostly due
macroinvertebrate-based indices have proved to be ef- to land reclamation, cage farming of fishes, illegal en-
fective measurements of the ecological status of transi- croachments, dredging, mangrove deforestation, waste
tional waters and coastal systems (McLusky and Elliott disposal, fish processing wastes and domestic sewage
2004), and hence, it is widely used for an ecosystem (Jayachandran and Bijoy Nandan 2012). However, hith-
health assessment (Bald et al. 2005; Blanchet et al. erto no information is available regarding the benthic
2008; Borja et al. 2008; Simboura and Zenetos 2002). macroinvertebrate response to various natural and an-
The present study emphasize on four commonly used thropogenic stresses in the KAE.
benthic biotic indices created based on the sensitivity of
ecological groups (EG) of macroinvertebrates such as Field and laboratory work
the benthic opportunistic polychaetes amphipods
(BOPA) index (Blanchet et al. 2008), AZTI’s Marine A total of seven study sites selected in the estuary for
Biotic Index (AMBI) (Borja et al. 2000), multivariate monthly field sampling (Fig. 1): St.1 was close to the
AMBI (M-AMBI) (Borja et al. 2008) and BENTIX estuary mouth, St.2 and 3 were in the middle zone, St.4
index (Simboura and Zenetos 2002) along with other and 5 were in the north arm of the estuary and St.6 and 7
benthic descriptors such as numerical density (ind. m−2), were located towards the high freshwater inputs. Month-
species number (S), Shannon diversity index (H′log2), ly sampling was conducted during the early morning
Margalef species richness (d), Pielou’s evenness index hours for 24 months, from July 2009 to June 2011 using
(J′), Simpson dominance (1-λ′) index and species com- the research vessel ‘King Fisher’. Monthly data were
position to characterize the benthic biocoenosis of grouped into seasons such as pre-monsoon (PRF [1st
Kodungallur-Azhikode estuary (KAE). Thus, the pres- year] and PRS [2nd year]: February–May; hot period
ent study intended (i) to evaluate the ecological position with less rainfall), monsoon (MNF [1st year] and MNS
of KAE for the first time, (ii) to compare the commonly [2nd year]: June–September; heavy rainfall) and post-
used biotic indices for benthic invertebrates in the coast- monsoon (PMF [1st year] and PMS [2nd year]:
al waters (AMBI, M-AMBI, BENTIX, BOPA along October–January; transitional period with intermediate
with others benthic parameters such as numerical rainfall) (Rehitha et al. 2018). Monthly rainfall data was
Environ Monit Assess (2020) 192: 626 Page 3 of 19 626

Fig. 1 Study sites selected in the Kodungallur-Azhikode estuary (KAE) for monthly field sampling

obtained from the India Meteorological Department was obtained from the Central Water Commission
(https://mausam.imd.gov.in/imd_latest/contents/rainfall (http://cwc.gov.in/get- hydrological-data). The water
information.php). The daily river discharge (RD) data samples were collected using a standard Niskin water
626 Page 4 of 19 Environ Monit Assess (2020) 192: 626

sampler (2.5 L). Sediment samples were collected using performed with SPSS v18.0. The Spearman rank-order
van Veen grab (0.04 m2). Environmental parameters correlation was performed to evaluate the correlation
such as temperature, pH, salinity and redox potential between the indices and sedimentary parameters. Ca-
(Eh) of water and sediments were recorded in situ using nonical correspondence analysis (CCA) was performed
a portable field analyser (Eutech ION 6+), and other using the software package CANOCO v4.5 (ter Braak
samples were kept in the icebox and taken into the and Smilauer 2002). Permutational multivariate analysis
laboratory for further analysis. In the laboratory condi- of variance (PERMANOVA) was performed to test the
tion, other physicochemical parameters were analysed null hypothesis of the study such as no differences
such as dissolved oxygen (DO) by using modified between dependent variables (community composition,
Winkler’s method and chlorophyll a (Chl-a) was esti- biotic indices and environmental parameters, a linear
mated by using the acetone extraction procedure model with spatial factor orthogonal at two nested tem-
(APHA 2005; Strickland and Parsons 1972). The anal- poral factors: stations (fixed, 7 levels: St.1 to St.7),
ysis of sediment grain size was performed by combined seasons (fixed, 6 levels: MNF, MFS, PMF, PMS, PRF
sieving and pipette methods (Carver 1971; Lewis 1984). and PRM) and months (random, 12 levels nested in
Organic carbon (OC) content of sediment was deter- season)). Each test was done using 9999 permutations
mined by modifying a wet oxidation method (El- of appropriate units. R packages ggplot2 in the CRAN
Wakeel and Riley 1957; Nelson and Sommers 1982; repository, ORIGIN v8.0 and MapInfo Professional
Trivedy and Goel 1986). Organic matter (OM) content v11.0 were used for graphical representation of data.
was also estimated from organic carbon values by mul- Diversity indices such as Margalef species richness
tiplying the Van Bemmelen factor of 1.724 (Trask 1939 (d), Shannon diversity index (H′), Pielou′s evenness (J′),
). For benthic macrofauna, three replicates were collect- and Simpson dominance (1-λ′) was calculated with
ed at each station with a van Veen grab (0.04 m2). PRIMER v6 + PERMANOVA software package by
Benthic samples were sieved through a 500-μm sieve, using the equations given below. Shannon diversity
and macroinvertebrates were preserved in 4% formalin index was calculated with log2.
for further identification (Eleftheriou and Mc Intyre
2005). In the laboratory, preserved samples were stained Total species ¼ S
Total individuals ¼ N
partially with Rose Bengal overnight then sorted and Margalef species richness ðd Þ ¼ ðS−1Þ=logðN Þ
identified to the possible lowest taxonomic level by Pielou’s evenness ð J 0 Þ ¼ H 0 =logðS Þ
using various online resources and published materials Shannon diversity index ðH 0 Þ ¼ SUM ðPi*logðPiÞÞ
(WoRMS 2017). Abundance data were presented as the Simpson dominance ð1−λ0 Þ ¼ 1−SUM Ni*ðNi−1Þ=ðN *ðN −1ÞÞ
density of individuals per square meter (ind. m−2) and
paper blotted wet weight biomass expressed as gram per The five ecological groups (EG) were assigned
m−2 (g m−2). based on the sensitivity of each species to an increas-
ing gradient of stress (http://www.azti.es v.5.0, species
Data analyses list updated in November 2014) in the benthic
environment (Borja et al. 2008; Borja et al. 2000) such
Multivariate analysis such as hierarchical cluster analy- as EGI (species highly sensitive to organic matter
sis based on Bray-Curtis similarity (for biotic parame- enrichment), EGII (species indifferent to enrichment),
ters) and Euclidean distance (for environmental param- EGIII (species tolerant to high organic matter enrich-
eters), similarity profile analysis (SIMPROF) and simi- ment), EGIV(second-order opportunistic species
larity percentage (SIMPER) analysis was done with favoured by excess organic matter enrichment) and
PRIMER v6 + PERMANOVA software package EGV (first-order opportunistic species preferred by
(Anderson 2001; Anderson et al. 2008; Clarke and excess organic enrichment). Similarly, since some of
Gorley 2006). Statistical analyses were conducted on the species in the KAE have not been listed in the
log-transformed biological data while environmental AZTI species list, the authors, therefore, followed the
data set log(X + 1) transformed and normalized to re- method described by Borja et al. (2008) when
duce the impact of dominant groups on analysis in the assigning new species (Feebarani et al. 2016). After
PRIMER v6 + PERMANOVA. Analysis of variance updating the species assignment, the percentage of
(ANOVA) and Spearman’s rank-order correlation were unassigned individuals ranged from 0 to 15.9%, with
Environ Monit Assess (2020) 192: 626 Page 5 of 19 626

a mean value of 2.79%. The multivariate AMBI (M- GI, and EGIII, EGIV and EGV were in GII (Simboura
AMBI) index was estimated by combining AMBI, and Zenetos 2002). The BENTIX index was calculated
species richness (S) and Shannon diversity index (H′ using the following equation:
log2) in factor analysis. This method relates biological
BENTIX ¼ 6GI þ 2GII
data from the field with reference conditions and it is
computed using AMBI software v5.0 (Bald et al. 2005
; Borja et al. 2008; Borja and Tunberg 2011). To
assess reference conditions of the benthic communities
living along with the salinity data, stations were clas- Results
sified based on salinity gradient (Borja et al. 2008). In
the absence of pristine environmental conditions, the Hydrography
reference values were taken by increasing the highest
diversity and richness values of all replicates at 15% The mean river discharge (RD) for the entire study
level (Borja and Tunberg 2011). Similarly, for the bad period was 252 ± 267 m3 s−1; the significant variation
status, reference was taken as same as azoic condition was observed between seasons (pseudo-F = 3.2457, p
(diversity and richness = 0 and AMBI = 6). Based on (perm) = 0.0001). Seasonally, monsoon season showed
the variation in salinity and environmental pressures, heavy discharge in relation to precipitation rate in the
the reference conditions for M-AMBI in KAE were set upper basins (606 ± 180 m3 s−1 for MNF and 473 ±
as follows: (i) St.7 and 6 (limno-polyhaline) with a 62 m3 s−1 for MNS). The mean of bottom water salinity
diversity of 3.55 and richness 14.95; (ii) St.5, 4, 3 and was 15.78 ± 9.90 PSU; the significant variation was
2 (oligo-polyhaline) with a diversity of 3.66 and rich- observed between stations (pseudo-F = 33.884, p
ness 19.55 and (iii) St.1 (meso-euhaline) with a diver- (perm) = 0.0001) and seasons (pseudo-F = 19.1, p
sity of 3.42 and richness of 13.80. In all cases, AMBI (perm) = 0.0001) (Fig. 2a). The lowest value for salinity
was 0. The AMBI index was calculated using the was observed at St.7 (11.78 ± 9.90 PSU) and highest at
following equation: St.1 (21.15 ± 9.75 PSU). The mean dissolved oxygen
(DO) for the entire estuary was 4.94 ± 1.11 mg L−1, the
AMBI ¼ 0EGI þ 1:5EGII þ 3EGIII þ 4:5EGIV significant variation was observed between stations
(pseudo-F = 2.8626, p (perm) = 0.0115) and seasons
þ 6EGV
(pseudo-F = 7.7388, p (perm) = 0.001) (Fig. 2b). Spa-
The BOPA index is an improved form of the benthic tially, a comparatively low mean value was observed at
opportunistic polychaetes amphipods ratio suggested by St.1 (4.57 ± 1.30 mg L−1), St.2 (4.67 ± 0.90 mg L−1),
Gesteira and Dauvin (2000). It uses the information on St.5 (4.77 ± 1.07 mg L−1) and St.4 (4.87 ± 1.05 mg L−1).
the total abundance of individuals and the frequency of The mean water column chlorophyll a (Chl-a) concen-
opportunistic polychaetes and amphipods, except the tration was 5.99 ± 4.48 mg m−3; in a spatial scale, St.5
opportunistic amphipod species belonging to the genus (7.73 ± 5.30 mg m−3) and St.7 (6.47 ± 5.47 mg m−3)
Jassa (EG V) (Blanchet et al. 2008). The BOPA index were recorded with high concentrations. No significant
was calculated using the following equation: variation was observed between stations (pseudo-F =
1.7731, p (perm) = 0.1085) and seasons (pseudo-F =
 
fP 2.3191, p (perm) = 0.0866) (Fig. 2c). The results of
BOPA index ¼ log þ1 PERMANOVA based on hydrographic parameters
fA
were varied significantly between all the stations (pseu-
where fP is the opportunistic polychaete frequency and do-F = 4.3403, p (perm) = 0.0001) and seasons (pseudo-
fA is the amphipod frequency. F = 10.665, p (perm) = 0.0001). Hierarchical cluster
The BENTIX index has been mainly used to assess analysis based on Euclidean distance and similarity
the general stress in an ecosystem and not capable to profile analysis (SIMPROF) indicated that all stations
differentiate natural and anthropogenic stress (Simboura behaved independently but riverine stations (St.6 and 7)
and Zenetos 2002). To calculate the BENTIX index, the grouped apart from other stations without any signifi-
same ecological groups were used; however, with some cant variation (0.72, p = 0.176). Chlorophyll a (Chl-a)
proportional differences, EG1 and EGII were placed in and salinity were the major factors for the separation of
626 Page 6 of 19 Environ Monit Assess (2020) 192: 626

Fig. 2 Spatio-temporal variation of environmental variables in KAE

stations. Similarly, seasons PRF and PRS have grouped was observed between stations (pseudo-F = 4.0023, p
apart from another season without significant variation (perm) = 0.0009) and seasons (pseudo-F = 2.4578, p
(2.58, p = 0.083). Salinity and dissolved oxygen were (perm) = 0.0626) (Fig. 2f). The sediment redox poten-
responsible for this separation. tial (Eh) values showed a reducing trend in all the
stations with a mean value of − 92.55 ± 78 mV; the
Sediment characteristics significant variation was observed between stations
(pseudo-F = 2.4758, p (perm) = 0.0246) but no vari-
The mean sediment temperature for the entire study ability between seasons (pseudo-F = 0.88193, p (perm)
period was 28.55 ± 1.70 °C; spatially St.5 (29.06 ± = 0.5226). Spatial variation of sediment Eh showed
1.43 °C) and St.7 (28.77 ± 1.88 °C) were recorded with highly reduced environment in St.6, St.7, St.2 and
the highest values; the significant variation was ob- St.5 as compared with that in St.4 and St.3 (Fig. 2d).
served between stations (pseudo-F = 3.9242, p (perm) The significant variation was observed in the sediment
= 0.0011) and seasons (pseudo-F = 3.8461, p (perm) = fraction between stations (sand: pseudo-F = 18.804, p
0.0137). The sediment pH was generally alkaline with (perm) = 0.0001, silt: pseudo-F = 16.21, p (perm) =
an overall mean of 7.81 ± 0.61 and ranging from 8.0 ± 0.0001 and clay: pseudo-F = 10.87, p (perm) = 0.0001).
0.73 (St.4) to 7.64 ± 0.44 (St.2); significant variation Seasonal variation was evident in silt distribution
Environ Monit Assess (2020) 192: 626 Page 7 of 19 626

(pseudo-F = 3.6741, p (perm) = 0.0168), while sand Community composition

(pseudo-F = 2.065, p (perm) = 0.1112) and clay (pseu-
do-F = 0.57691, p (perm) = 0.7123) distribution were The benthic macroinvertebrates of KAE were represent-
not varied significantly. Overall, high sand fraction was ed by 75 species, polychaetes dominated with 33 spp.,
observed in the estuarine sediment (mean 81.61 ± followed by malacostracans with 26 spp., mostly am-
16.59%), and spatially, St.4, St.3, St.1 and St.5 were phipods (9 spp.), decapods (8 spp.) and isopods (4 spp.)
exhibited comparatively higher sand fraction compared (Fig. 4). Dominant polychaete species were Prionospio
with St.6, St.2 and St.7, while high silt and clay con- cirrifera, Capitella sp. and Notomastus species. The
tents were observed in the sediment of St.6 and St.2 numerically dominant malacostracans were amphipod
(Fig. 3). OM was 16.10 ± 12.30 g kg−1 with high values Americorophium triaeonyx and isopod Cirolana
at St.6, St.2 and St.7. Relatively low OM content was fluviatilis. The numerically dominant molluscans were
recorded at St.4, St.1, St.3 and St.5; the significant Arcuatula senhousia, Marcia recens and Villorita
variation was observed between stations (pseudo-F = cyprinoides. The other group was mainly contributed
60.505, p (perm) = 0.0001) and seasons (pseudo-F = by hydrozoan colony of Obelia bidentata. In a spatial
4.2465, p (perm) = 0.0122) (Fig. 2e). In the results of scale, relatively low polychaete species count was re-
PERMANOVA based on overall sediment parameters corded at St.7 (14 spp.) while moderately high species
showed spatial (pseudo-F = 12.907, p (perm) = 0.001) counts have been recorded at St.4 (21 spp.), St.5 (21
and temporal variation (pseudo-F = 2.4161, p (perm) = spp.) and St.6 (21 spp.). There is no significant variation
0.002). However, hierarchical cluster analysis based on in malacostracan species count recorded between sta-
Euclidean distance and SIMPROF showed significant tions; St.2, 5 and 7 recorded with 14 spp., while St.1, 3,
variation between some stations (1.45, p = 0.001). Sta- 4 and 6 had 15 spp. recorded. The molluscan species
tions five and six behaved independently, while stations count was varied from 1 sp. in St.6 to the highest
one, three and four were grouped together (0.7, p = number of 11 spp. at St.4 and St.6 (Fig. 5).
0.258); similarly, stations two and seven (0.74, p = In the results of PERMANOVA, based on the abun-
0.10) formed another cluster. Organic matter (OM), dance data showed a significant variability in the benthic
clay and silt contents were the major factor that sepa- species assemblage between stations (pseudo-F =
rated stations. Seasons behaved independently, but 6.0387, p (perm) = 0.0001) and seasons (pseudo-F =
monsoon seasons (MNF and MNS) grouped apart from 1.867, p (perm) = 0.0004). Hierarchical cluster analysis
other stations without any significance (1.75, p = based on Bray-Curtis similarity and similarity profile
0.387). Differences in sediment ph, Eh and silt contents analysis (SIMPROF) grouped seven stations in the
were the major factors for the separation of seasons KAE into two groups of stations (STA and STB;
(Supplementary Table 1). 47.19%, p < 0.05) based on the assemblage pattern of

Fig. 3 Sand, silt and clay

contents observed in the sediment
fraction of KAE
626 Page 8 of 19 Environ Monit Assess (2020) 192: 626

Fig. 4 Contribution of different macroinvertebrate groups to the total density of benthic macroinvertebrate in KAE

macroinvertebrates. The STA group was composed of Overall comparison of benthic biotic indices showed
stations one, three and four (68.12%, p < 0.5), while the a spatial (pseudo-F = 5.1255, p (perm) = 0.0001) vari-
STB group was represented by stations two, five, six ations; no significant variation was noticed between
and seven, with 50.25% similarity (p < 0.5). Similarity seasons (pseudo-F = 1.7442, p (perm) = 0.0801). The
percentage (SIMPER) analysis was performed to under- hierarchical cluster analysis based on Euclidean distance
stand the species responsible for clustering. The eight and SIMPROF showed significant variation between
dominant and frequent species were responsible for the riverine stations (seven, six and two) and other stations
formation of the STA group and they were A. triaeonyx, (1.09, p = 0.06) (Supplementary Table 2).
C. fluviatilis, O. bidentata, Grandidierella megnae,
A. senhousia, Capitella sp., M. recens and Cyathura Richness/diversity indices
indica (0.90%), while twelve species accounted for the
formation of cluster STB and they were P. cirrifera, The macroinvertebrate Margalef species richness (d)
Capitella sp., Notomastus sp., Dendronereis aestuarina, in KAE varied from 0.65 ± 0.43 in St.7 to 1.24 ± 0.36
Lumbriconereis notocirrata, A. triaeonyx, O. bidentata, in St.4 with an overall mean of 0.84 ± 0.40, and var-
C. fluviatilis, Victoriopisa chilkensis, Glycera iations between seasons were significant (pseudo-F =
tridactyla, G. megnae and Nassodonta insignis. Simi- 5.1255, p (perm) = 0.0001). Seasonally, it varied from
larly, SIMPROF grouped six seasons (3 seasons × 0.78 ± 0.42 in MNS to 0.86 ± 0.40 during PMF; how-
2 years) in the KAE into two groups of seasons (SSA ever, seasonal variation was not statistically signifi-
and STB; 52.46%, p < 0.05). The SSA group was com- cant (pseudo-F = 1.7442, p (perm) = 0.074) (Fig. 6d).
posed of seasons MNF, MNS, PMF and PMS (65.24%, A relatively low Pielou’s evenness index (J′) was
p < 0.5), while the SSB group was represented by PRF recorded during the study with a mean value of 0.70
and PRS with 50.25% similarity (62.36%, p < 0.5). The ± 0.20, and it varied from 0.60 ± 0.23 in St.3 to 0.78 ±
abundance of fourteen species contributed extensively 0.17 in St.6 (between stations, pseudo-F = 5.1255, p
to the average dissimilarity between two groups (SSA (perm) = 0.001). Seasonally, it varied from 0.61 ±
and SSB). They were A. triaeonyx (38.80%), 0.22 in PMF to 0.80 ± 0.12 in PRF (between seasons,
O. bidentata, A. senhousia, P. cirrifera, Notomastus pseudo-F = 1.7442, p (perm) = 0.082). The annual
sp., Pista indica, Ceratonereis costae, C. fluviatilis, value of the Shannon index [H′log2] was highest
M. recens and Capitella sp. (Fig. 5). during the 1st year (mean 1.93 ± 0.68) compared with
Environ Monit Assess (2020) 192: 626 Page 9 of 19 626

Fig. 5 Seasonal variation of benthic macroinvertebrate species density in KAE

that in the 2nd year period (mean 1.60 ± 0.86) (Fig. 1.7442, p (perm) = 0.076). The mean Simpson dom-
6c). Seasonally, the lowest values were recorded dur- inance (1 − λ′) index for macroinvertebrate commu-
ing PMS (mean 1.50 ± 0.89) and highest at PRF nities in the study area varied from 0.51 ± 0.24 in St.1
(mean 2.11 ± 0.60) with the overall mean of 1.77 ± to 0.65 ± 0.15 in St.6 (between stations, pseudo-F =
0.79 (between stations, pseudo-F = 1.7442, p (perm) 1.7442, p (perm) = 0.001). Seasonally, it varied from
= 0.001). Spatial diversity varied from the lowest 0.50 ± 0.27 during PMS to 0.69 ± 0.13 at PRF (be-
value in St.1 (mean 1.50 ± 0.75) to highest in St.4 tween seasons, pseudo-F = 1.7442, p (perm) = 0.093)
(mean 2.07 ± 0.84) (between seasons, pseudo-F = (Tables 1, 2 and 3).
626 Page 10 of 19 Environ Monit Assess (2020) 192: 626

Fig. 6 Spatio-temporal variation of macroinvertebrate based univariate indices of KAE

Benthic opportunistic polychaetes amphipods index 0.11544 ± 0.11495 were recorded for the 2nd year,
when compared with the value of 0.10217 ± 0.10282
In the present study, the mean BOPA index for KAE in the 1st year. Seasonally, BOPA was relatively higher
was 0.10880 ± 0.10893 and annually higher values of during MNF (0.12882 ± 0.11731) followed by PMS

Table 1 Results of Spearman’s rank-order correlation between the indices and the environmental variables

N ind. m−2 g m−2 S D H′ BOPA AMBI BENTIX M-AMBI

Salinity .031 − .005 .034 .043 − .036 − .194 − .190 .176 .054
DO − .011 − .001 − .087 − .091 − .121 .064 .178 − .239 − .117
OM − .257 − .301 − .363 − .347 − .175 .305 .346 − .239 − .362
Sed. Eh .022 .192 .051 .098 − .016 − .164 − .127 .104 .106
Sed. pH − .029 .214 .025 .071 .084 − .093 − .211 .119 .155
Sand .232 .216 .291 .246 .172 − .243 − .265 .159 .282
Silt − .179 − .154 − .264 − .226 − .191 .184 .207 − .128 − .261
Clay − .204 − .188 − .222 − .179 − .094 .201 .221 − .165 − .196

Statistical significance (p ≤ 0.05) is italicized

Environ Monit Assess (2020) 192: 626 Page 11 of 19 626

Table 2 Results of Spearman’s rank-order correlation between was relatively higher during PMS (3.14 ± 1.19)
biotic indices–derived ecological quality (EcoQ) status
followed by MNF (2.85 ± 1.18), PRS (2.80 ± 0.97)
classifications
and MNS (2.71 ± 1.24), PMF (2.39 ± 1.45) and PRF
BENTIX AMBI BOPA H′ S (2.28 ± 1.22) (between seasons, pseudo-F = 1.7442, p
(perm) = 0.087). On a spatial scale, AMBI values
MAMBI .483 − .443 − 0.13 .789 .575
were higher in the STB group of the stations such as
BENTIX − .783 − .483 .270 − 0.01
St.6 (3.21 ± 1.17), St.2 (3.13 ± 1.33), St.7 (3.09 ±
AMBI .718 − 0.052 − 0.053
1.42) and St.5 (2.78 ± 1.22), compared with those in
BOPA .196 0.104 the STA group of stations, St.3 (2.33 ± 0.79), St.1
H′ .430 (2.26 ± 1.21) and St.4 (2.06 ± 0.92). The index values
Statistical significance (p ≤ 0.05) is italicized of STA stations reported undisturbed to the slightly
disturbed condition while those in the STB stations
(0.12011 ± 0.12426), PRS (0.11318 ± 0.11042), MNS ranged from a slightly disturbed to moderately dis-
(0.11304 ± 0.11379), PRF (0.09264 ± 0.09555) turbed status. Among all the sampling locations, St.6,
(0.08504 ± 0.09206) (between seasons, pseudo-F = 2, 7 and 5 exhibited a high AMBI index indicating a
1.7442, p (perm) = 0.097). Spatially, the STB group of poor environmental conditions (between stations,
stations had relatively higher value (St.6 (0.18529 ± pseudo-F = 1.7442, p (perm) = 0.001) (Figs. 7 and
0.09007), St.5 (0.16571 ± 0.09855), St.7 (0.14758 ± 8c; Tables 1, 2 and 3).
0.11508) and St.2 (0.13592 ± 0.11349)), compared with
the STA group (St.1 (0.06083 ± 0.09239), St.4 BENTIX
(0.03475 ± 0.05995) and St.3 (0.03154 ± 0.06248) (be-
tween stations, pseudo-F = 1.7442, p (perm) = 0.001). The mean BENTIX index was 3.62 ± 1.36, and annu-
The index values of STA stations indicated good to ally, comparatively low value was observed for the
moderate condition, while those in the STB stations 2nd year (3.38 ± 1.34) than that for the 1st year (3.86
ranged from a moderate or poor condition. Among all ± 1.35). Temporarily, BENTIX had relatively low
the sampling locations, St.6, 5, 7 and 2 exhibited higher values at PMS (3.11 ± 1.46) followed by MNF (3.29
BOPA index, and the values even reached > 0.30 indi- ± 1.12), MNS (3.44 ± 1.32) and PRS (3.58 ± 1.22),
cating the poor environmental conditions at these sta- PMF (3.84 ± 1.57) and PRF (4.45 ± 1.10) (between
tions (Figs. 7 and 8b; Tables 1, 2 and 3). seasons, pseudo-F = 1.7442, p (perm) = 1.7442).
Spatially, BENTIX values were lower in the STB
AZTI’s Marine Biotic Index group (St.7 (3.24 ± 1.44), St.2 (3.27 ± 1.39), St.5
(3.77 ± 1.28) and St.6 (3.40 ± 1.10)), compared with
The mean AMBI index for KAE was 2.69 ± 1.23. those in the STA group (St.1 (3.82 ± 1.60), St.3 (3.84
Annually, a relatively higher value was depicted in ± 1.28), St.4 (3.97 ± 1.35)) (between stations, pseudo-
the 2nd year (2.88 ± 1.14) compared with that in the F = 1.7442, p (perm) = 0.001) (Figs.7 and 8a;
1st year (2.51 ± 1.30). Seasonally, the AMBI index Tables 1, 2 and 3).

Table 3 Ecological quality (EcoQ) status classes used to classify index values in this study

EcoQ status

High Good Moderate Poor Bad

H′log2 >4 4–3 3–2 2–1 <1 Blanchet et al. 2008

BOPA 0.00–0.045 0.045–0.139 0.139–0.193 0.193–0.267 0.267–0.301 Dauvin and Ruellet 2007
AMBI 0.0–1.2 1.2–3.3 3.3–4.3 4.3–5.5 > 5.5 Borja et al. 2000
M-AMBI > 0.77 0.77–0.53 0.53–0.38 0.38–0.20 < 0.20 Muxika et al. 2007
BENTIX 6–4.5 4.5–3.5 3.5–2.5 2.5–2.0 0 Simboura and Zenetos 2002
626 Page 12 of 19 Environ Monit Assess (2020) 192: 626

Fig. 7 Percentage contribution of different ecological groups in KAE between stations and seasons

Multivariate AMBI pseudo-F = 1.7442, p (perm) = 0.001) (Figs. 7 and 8b;

Tables 1, 2 and 3).
The mean M-AMBI for KAE was 0.4825 ± 0.1465 with
minimal annual variation, and that was 0.4540 ± 0.1515 Relationship between environmental variables
during the 2nd year and 0.5107 ± 0.1364 for the 1st and benthic descriptors
year. At seasonal scale, relatively lower value was ob-
served for PMS (0.4352 ± 0.1481) and PRS (0.4629 ± For the CCA analysis, the Monte Carlo test was run
0.1470) and MNS (0.4640 ± 0.1561) followed by PMF to identify significant environmental variables
(0.4961 ± 0.1604), MNF (0.5092 ± 0.1252) and PRF influencing the observed variability. Salinity, DO,
(0.5268 ± 0.1252) (between seasons, pseudo-F = OM, sediment Eh, sediment pH and sand were iden-
1.7442, p (perm) = 0.084). Spatially, the lowest values tified as important variance descriptors (F-ratio =
were recorded for the STB group of St.2 (0.3892 ± 1.350, P value = 0.0420 for all axis). Sixty-six
0.1588), St.7 (0.4291 ± 0.1760), St.6 (0.4551 ± 1106) percentage of biological and synthetic index vari-
and St.5 (0.4941 ± 0.1038), compared with those for ability was explained at the first four axes. The first
the STA group St.4 (0.6050 ± 0.1104), St.3 (0.5039 ± and the second canonical axes explained together up
0.12451) and St.1 (0.5003 ± 0.1395) (between stations, to 47.1% of the total variance of 38.4% and 8.7%.
Environ Monit Assess (2020) 192: 626 Page 13 of 19 626

Fig. 8 Assessment results of benthic indices between stations and seasons

Samples from the northern arm (St.3, 4 and 5), river Discussion
head region (St.6 and 7) and estuarine mouth re-
gions (St.1, 2 and 3) were grouped separately Estuarine ecosystems are increasingly become polluted
(Fig. 9). Sand percentage showed a negative relation and degraded by human activities; therefore, many re-
with OM and clay, while AMBI and BOPA values searchers have begun to study various aspects of impacts
indicated a positive relationship with environmental on these critical ecosystems to evaluate and provide scien-
factors such as clay and OM together with increased tific evidence to government and private bodies to manage,
abundance of opportunistic polychaete species like protect and recover these critical ecosystems from further
Prinospio cirrifera and Capitella sp. BENTIX damage (Ajmal Khan et al. 2014; Anu et al. 2016; Anu
values indicated its affinity with salinity and sand, et al. 2018; Don Xavier et al. 2019; Jayachandran et al.
moreover values increased towards bar mouth region 2019b; Mulik et al. 2017; Watson et al. 2018). In Indian
(St.1 and 2), especially during post and pre- waters, marine biotic index–based studies on coastal and
monsoon period. M-AMBI remained intermediate estuarine have increased significantly over the last few
in both domains. OM, clay and silt content mainly years (Ajmal Khan et al. 2014; Asha 2017; Equbal et al.
explained increased ecological disturbances from 2018; Equbal et al. 2017; Feebarani 2009; Mulik et al.
natural and anthropogenic sources that were related 2017; Naidu et al. 2018; Rehitha et al. 2017; Sigamani
to moderate to bad quality assigned by high AMBI et al. 2015; Sivadas et al. 2016; Sivaraj et al. 2014). In the
and BOPA scores and low M-AMBI and BENTIX present study, the overall result of multivariate indices
scores. tested in the Kodungallur-Azhikode estuary (KAE)
626 Page 14 of 19 Environ Monit Assess (2020) 192: 626

Fig. 9 CCA triplot of biological,

environmental and synthetic
index variability (Ame.:
Americorophium triaeonyx,
ObBi.: Obelia bidentata, Arc.:
Arcuatula senhousia,
Pri.: Prionospio cirrifera, Den.:
Dendronereis aestuarina and
Cap.: Capitella sp.)

showed AMBI having a ‘good to moderate’ condition, M- clay sediment of the STB group of stations. Species
AMBI ‘good to poor’ condition, BENTIX ‘high to mod- representing EGIV is second-order opportunistic, while
erate’, high to poor condition in BOPA and ‘moderate to that of EGV belongs to first-order opportunistic species
poor’ condition in univariate Shannon diversity index. A that proliferate with enrichment of organic matter. At the
recent study on benthic biotic indices in the nearby Cochin same time, species that belongs to EGI such as Diopatra
estuary has also indicated ‘moderate-poor’ ecological con- neapolitana was recorded from sandy sediments of the
dition (Feebarani et al. 2016). As mentioned above, some STA group of stations in the KAE (Bald et al. 2005).
of the indices tested during the current study have shown a Seasonally, no significant variation was observed in the
wide range of variations, such as high to poor condition in spatial pattern of multivariate indices tested while species
BOPA and moderate to poor condition in the Shannon composition was slightly varied with salinity changes
diversity index. The most dominant species in the current and sediment disturbance from heavy river discharge.
study location was opportunistic amphipod, During the post-monsoon period, O. bidentata of EGII
Americorophium triaeonyx, and it belongs to ecological was abundant while A. triaeonyx of EGIII dominated
group three (EGIII), and other dominant species were during the other seasons.
Arcuatula senhousia (EGIII), Cirolana fluviatilis (EGII), The BOPA index is mainly focused on the preference
Paraprionospio sp. (EGIV), Capitella sp. (EGV), of opportunistic polychaetes in the organically enriched
Ceratonereis costae (EGII), Notomastus sp. (EGIII), sediments (Blanchet et al. 2008). The sensitivity of amphi-
Marcia recens (EGI) and Obelia bidentata (EGII). These pods to pollution is widely used in ecological monitoring
ecological groups are indifferent or tolerant to high or- programmes around the globe including Indian waters
ganic matter enrichment. However, opportunistic poly- (Blanchet et al. 2008; Sivadas et al. 2016). BOPA index
chaete species such as Prionospio cirrifera which be- was applied to seven stations in the estuary to understand
longs to ecological group four (EGIV) and Capitella sp. different perturbations (cage farming of fishes, aquaculture
which belongs ecological group five (EG V) were repre- and agriculture activities in the adjacent ponds, sewage
sented by a huge number in the organic matter–enriched discharge etc.) in the KAE. The significant difference in
Environ Monit Assess (2020) 192: 626 Page 15 of 19 626

the BOPA index was observed among stations; the value communities is fundamental (Borja et al. 2000); howev-
for the entire estuary indicated high to poor ecological er, KAE was not fully exposed to a high level of urban
condition. The pattern of disturbance closely matched with effluent as compared with Cochin estuary.
the spatial grouping pattern of macroinvertebrate assem- The biotic index BENTIX is based on the sensitivity or
blages in the estuary. The STA group of stations (St.1, 3 tolerance of two ecological groups (Simboura and Zenetos
and 4) are dominated with a sandy substrate and a moder- 2002). According to Simboura et al. (2007), BENTIX is
ate level of organic content indicates high to good condi- best for assessing the long-term trends of decline or recov-
tions, while the STB group (St.2, 5, 6 and 7) demonstrated ery status of an ecosystem. Spatial variation of BENTIX in
moderate to poor conditions. In stations two and five, cage the estuary maintained the trend of other indices employed.
farming of carnivore fish, Lates calcarifer, supplies organ- In this index, the STA group of stations had high to
ic matter to adjacent areas which also received supply from moderate ecological status. The STB group stations
traditional aquaculture farms. Within the latter group, sta- showed good to moderate disturbance as noticed in the
tions six and seven also indicated maximum disturbance; different indices. However, some of the STB group of
they receive excess organic material from upper river stations even occasionally displayed bad ecological status.
basins during the heavy river discharge period. The supply Seasonally, the values for the entire estuary depicted rela-
of excess organic material and subsequent degradation tively high disturbance in monsoon and post-monsoon
process also decreased the ecological quality of already (moderate condition) compared with those in pre-
disturbed stations in the KAE such as stations two, five and monsoon.
six. However, different studies have challenged the pollu- According to Borja et al. (2000), benthic communities
tion sensitivity of species from the same taxonomic group responded to changes in environmental quality in three
having different responses (Andrade and Renaud 2011). different ways: an increase in species abundance, diversity,
Riera and de-la-Ossa-Carretero (2014) state that the BOPA and variation of dominant species from tolerant to sensitive
index is more suitable for the heavily impacted environ- to pollution. In M-AMBI, pressure gradients are also con-
ments than other areas of anthropogenic disturbances; sidered before assigning the ecological status. According
however, in the present study, BOPA separated variation to Borja et al. (2009), biotic indices AMBI and M-AMBI
between stations with a mild level of organic enrichment. can discriminate different anthropogenic distresses in an
Widely accepted indices such as the AZTI’s Marine ecosystem such as aquaculture effluent impacts, nutrient
Biotic Index (AMBI) were also performed in the KAE loading, eutrophication, anoxia and hypoxia, and oil and
(Ajmalkhan et al. 2004; Equbal et al. 2017; Sivadas et al. industrial pollution (Borja et al. 2009; Don Xavier et al.
2016). The advantage of AMBI is that it does not require 2019; Pinto et al. 2009; Santibañez-Aguascalientes et al.
a reference station for comparison. In the present study, 2018; Vineetha et al. 2020). In the M-AMBI index based
the AMBI index showed a similar pattern to the BOPA on the factorial analysis of Shannon’s diversity, richness
index but most of the values between good to moderate and AMBI index, the ecological status of KAE ranged
condition. Accordingly, the STA group of stations ex- between good and poor conditions. This index has also
hibited good condition compared with the STB group. been validated as an effective ecological tool for assessing
The proliferation of opportunistic species belonging to the ecosystem health status of benthic communities of
EGIV and EGV is responsible for the high AMBI value diverse geographical locations under varying anthropogen-
(Bald et al. 2005). Similarly, the AMBI index showed ic pressures, ranging from tropical conditions to higher
that the Cochin estuary had moderately disturbed status, latitudes (Borja and Tunberg 2011; Feebarani et al. 2016;
Vellar estuary was undisturbed and Uppanar estuary had Sigovini et al. 2013; Spagnolo et al. 2014). Many studies
polluted status (Ajmalkhan et al. 2004; Feebarani et al. have performed M-AMBI to evaluate the ecological con-
2016). In the Vellar-Coleroon estuarine system, the mod- dition of transitional and coastal waters and observations
erately disturbed conditions (AMBI between 3.45 and varied in place and time. A high to good ecological status
3.72) were observed at the discharge point of shrimp (0.9 ± 0.06) was observed in Vellar estuary and a poor to
farms and dredging stations (Sigamani et al. 2015). In bad status at Uppanar estuary (0.22 ± 0.04) (Ajmal Khan
this biotic index, assessing the health of the ecosystem et al. 2014), while the moderate condition was reported in
based on organic matter input either from sewage or Cochin estuary (Feebarani et al. 2016). Similar to all the
eutrophication and successive assemblage pattern of a other three indices used in the present study, M-AMBI
different ecological group of macroinvertebrate showed the same pattern in spatial scale. However, the
626 Page 16 of 19 Environ Monit Assess (2020) 192: 626

ecologically good status was only observed in the stations and M-AMBI. The upstream southern zone significantly
having high sandy sediment with low OM and all other influenced the ecology of the estuary by freshwater
stations in the estuary was displayed poor to moderate discharge from the Periyar and Chalakudy rivers. Some
ecological status. It was also noticed that station two in of the stations in the middle and northern part are
the middle zone of an estuary with muddy substratum experiencing various pressures from aquaculture and
depicted relatively low ecological status (moderate) due other anthropogenic disturbances. This assessment is
to increased accumulation of organic matter from fish expected to be useful for developing a monitoring and
cages and riverine input. management strategy to protect this important coastal
All indices tested in the KAE behaved similarly with ecosystem.
slight variations in the range. Multivariate indices such
as BENTIX, AMBI, M-AMBI and BOPA were corre- Acknowledgements This work forms part of the research pro-
lated with each other except BOPA and M-AMBI. ject entitled ‘Ecology and fish production potential of the
Kodungallur - Azhikode backwater ecosystem’ funded by the
Some studies showed contrasting results when compar-
Kerala State Council for Science, Technology and Environment
ing indices H′log2, AMBI, M-AMBI, BOPA and (KSCSTE), and the authors are thankful for their financial assis-
BENTIX (Spagnolo et al. 2014). Many of the earlier tance. Authors are also thankful to the Head, Department of
studies warned the use of biotic indices when commu- Marine Biology, Microbiology and Biochemistry, Cochin Univer-
sity of Science and Technology, for providing necessary facilities.
nities dominating tolerant and opportunistic species or
The first author is grateful to Ángel Borja, AZTI, Marine Research
correlation between species diversity and natural stress Division, Spain, for his pieces of advice and help for this study.
were high because these indices tend to fail at such The reviewers of the manuscripts are acknowledged for their
conditions (Reizopoulou et al. 2014). Besides, the pre- constructive criticism for improving the manuscript.
cise taxonomic identification and functional trait evalu-
ation have played a key role in the accurate valuation of Funding This study was funded by the Kerala State Council for
ecological status; in the naturally disturbed estuarine Science, Technology and Environment (KSCSTE), Kerala, India.
ecosystems, critical evaluation is necessary for the better
Compliance with ethical standards
performance to differentiate influence on natural and
anthropogenic changes (Mulik et al. 2017). According Conflict of interest The authors declare that they have no con-
to Sivadas et al. (2016), these benthic indices originally flict of interest.
developed for temperate benthic systems are efficient in
Indian coastal waters; however, complementary use of a
different index is recommended for an accurate assess-
ment and validation of ecological quality.

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