macrofauna epibentónica tsunami chile

Mar Biol
DOI 10.1007/s00227-013-2370-x
Original Paper
Epibenthic macrofaunal community response after
a mega‑earthquake and tsunami in a shallow bay
off central‑south Chile
Eduardo Hernández‑Miranda · José Cisterna ·
Ernesto Díaz‑Cabrera · Rodrigo Veas ·
Renato A. Quiñones
Received: 7 May 2013 / Accepted: 10 December 2013
© Springer-Verlag Berlin Heidelberg 2013
Abstract On February 27, 2010, the world’s sixth strongest earthquake on record (8.8 Mw) and tsunami hit central
Chile. We assess the response of the epibenthic macrofaunal community following this event in Coliumo Bay, one
of the areas most affected by this mega-perturbation. The
indicators of aggregate and compositional variability show
that 3 years after this event, the community appears to have
undergone the following dynamics: (1) At an inter-annual
timescale, the community (both in density and biomass)
shifted through different structures with apparent directionality; (2) Oceanographic and biological seasonality had a
strong cyclical influence on the inter-annual community
response; (3) There was spatial homogenization of the
community over time (i.e., recovery of diversity), probably
promoted by the ecological functionality of scavenger species (i.e., crab Cancer coronatus and snail Nassarius spp.)
Communicated by M. G. Chapman.
Electronic supplementary material The online version of this
article (doi:10.1007/s00227-013-2370-x) contains supplementary
material, which is available to authorized users.
E. Hernández‑Miranda (*) · J. Cisterna · E. Díaz‑Cabrera ·
R. Veas · R. A. Quiñones
Programa de Investigación Marina de Excelencia (PIMEX),
Facultad de Ciencias Naturales y Oceanográficas, Universidad de
Concepción, Concepción, Chile
e-mail: [email protected]
E. Hernández‑Miranda · R. A. Quiñones
Interdisciplinary Center for Aquaculture Research (INCAR),
Casilla 160‑C, Universidad de Concepción, Concepción, Chile
J. Cisterna · R. A. Quiñones
Graduate Program in Oceanography, Department
of Oceanography, Casilla 160‑C, University of Concepción,
Concepción, Chile
and by the proportional increase in non-dominant species;
(4) Bathymetry and bottom dissolved oxygen also played
significant roles in the spatial structure of this community;
(5) Three years after the perturbation, total density and total
community biomass were still considerably below those
described under unperturbed conditions, mainly associated with the decrease in density and biomass of dominant
species. Therefore, in spite of this apparent community
compositional recovery, the aggregate variability currently
remains below the levels reported prior to the effect of
the mega-earthquake and tsunami. These results provide
evidence that supports both the Cross-Scale Resilience
Hypothesis and the Response Diversity Hypothesis.
Introduction
On 27 February 2010, the Maule mega-thrust earthquake
(27F) struck the coast of central Chile in the southern
Pacific Ocean. This event had a registered moment magnitude of 8.8 (Mw), making it the sixth largest event in the
seismological record (Sobarzo et al. 2012; USGS 2013).
The hypocenter (36°29′S, 73°24′W) was located in the
ocean at a depth of 6.2 km, with a north–south rupture
zone of approximately 500 km, affecting the ConcepciónConstitución seismic gap (Ruegg et al. 2009) off central
Chile (Farías et al. 2010; Madariaga et al. 2010; Vargas
et al. 2011). 27F generated a maximum coastal horizontal displacement of almost 5 m, with a 2.4 ± 0.2 m maximum vertical rise of the sea floor (Vargas et al. 2011). The
waves generated by 27F propagated rapidly due to the shallow bathymetry of this coastal zone (600 km h−1 to the
north and 300 km h−1 to the south), and with short periods
(~50 min to the north and ~130 min to the south), generating a tsunami with waves of maximum height of almost
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Mar Biol
14 m to the north of the epicenter and 8 m to the south
(Vargas et al. 2011; Vigny et al. 2011; Sobarzo et al. 2012).
The mega-earthquake and tsunami devastated coastal areas
along approximately 500 km of coastline, strongly modifying intertidal and subtidal environments. Immediate and
posterior effects described for this zone include the following: the elevation of rocky intertidal and subtidal areas,
which produced massive mortality of organisms (Castilla
et al. 2010); strong modifications of the geomorphology of
sandy beaches, negatively affecting populations of intertidal organisms (Jaramillo et al. 2012; Veas et al. 2013);
and a strong negative effect on artisanal fisheries due to the
temporary disappearance of commercial species (Marin
et al. 2010), probably associated with the mass stranding
of organisms observed immediately following the tsunami.
These negative ecological impacts on the ecosystem, which
were initially detected, will most likely have repercussions
for years (Nelson and Manley 1992; Castilla et al. 2010;
Turner 2010; Jaramillo et al. 2012). One of the coastal areas
most affected by the mega-earthquake and tsunami was
Coliumo Bay. This bay was struck by at least four waves,
which arrived between 03:54 and 06:40, 20 min to 3 h after
the earthquake (Sobarzo et al. 2012). This series of waves
of 6–8 m height (Vargas et al. 2011) emptied the bay completely at least three times, eroding the sea floor, strongly
impacting sedimentary beds, and drastically modifying the
habitat of resident species. The sea floor in Coliumo Bay
was raised by an estimated average of 0.5 m (Castilla et al.
2010; Vargas et al. 2011; Vigny et al. 2011; Sobarzo et al.
2012).
Earlier studies of the sedimentary sea floor of Coliumo
Bay reported the presence of a diverse epibenthic macrofaunal community composed of more than 70 species,
dominated mainly by scavenger mollusks and crustaceans,
along with bentho-demersal fish (Hernández-Miranda et al.
2010, 2012a, b). Prior to 27F, the temporal dynamics of
this community were driven by two related oceanographic
processes: coastal upwelling and natural hypoxic events.
Coastal upwelling is a typical process in this area of continental shelf of the southeast Pacific Ocean. It displays
high seasonal variability with intermittent events, which are
more frequent and intense in spring and summer (Shaffer
et al. 1999; Sobarzo et al. 2007), and is the physical motor
behind the high seasonal primary and secondary productivity in this area of the Humboldt Current System (Fossing
et al. 1995; Daneri et al. 2000, 2012; Sobarzo et al. 2007).
As a result of the upwelling process, equatorial subsurface
waters with low dissolved oxygen levels (<0.5 ml O2L−1)
intrude into the coastal zone (Quiñones et al. 2010). In
extreme cases, this hypoxic water produces mass mortality and stranding of organisms, mainly in semi-enclosed
bays (Ahumada and Arcos 1976; Hernández-Miranda et al.
2010). Hernández-Miranda et al. (2010, 2012a) suggested
13
that the resident epibenthic macrofaunal community of
Coliumo Bay is highly resilient to severe natural perturbations, such as hypoxia. This hypothesis is based on the
community response observed following an intense natural
hypoxic event, which occurred in January 2008. Immediately after this event, the community suffered a sharp
decrease in total density, total biomass, and diversity, which
was rapidly countered by the recovery of these variables in
less than 3 months. In the 2 years that followed, however,
the structure of the community was modified from being
initially dominated by the decapod C. coronatus to being
dominated by the gastropod Nassarius spp.; both species
are defined as scavengers/carnivores (Gutiérrez et al. 2000;
Laudien et al. 2007). This short-term recovery (i.e., months)
and the subsequent inter-annual response appear to be associated with the seasonal reproductive cycles of the majority
of species in this community (i.e., demographic processes)
and the high connectivity with the adjacent coastal area via
larval transport (Hernández-Miranda et al. 2012a). These
biological/ecological processes are ultimately linked to the
seasonal oceanographic conditions characteristic of this
coastal zone in the southeast Pacific Ocean.
Building on previous studies, Coliumo Bay provides a
unique opportunity to study the dynamics of the epibenthic macrofaunal community after the mega-earthquake
struck and to assess whether its response was similar to that
observed after the strong perturbation caused by the severe
natural hypoxic event in January 2008. We examined two
main hypotheses: (i) the inter-annual dynamics of the epibenthic macrofaunal community after 27F was driven
by the seasonality of biological/ecological processes and
oceanographic conditions, and (ii) the community dynamics following 27F shifted to a structure similar to that found
in 2007, before the effect of the strong natural hypoxic
event (i.e., return to unperturbed condition).
Thus, the objectives of this study were as follows: (1)
temporally assess the aggregate and compositional variability of the community following 27F, (2) assess the role
of the spatial factor within Coliumo Bay (i.e., bathymetric
response) on temporal dynamics, (3) identify the dominant
species in the community after 27F and their spatial and
temporal dynamics, and (4) verify whether after 27F the
community structure approximated that reported prior to
the severe natural hypoxia perturbation.
Materials and methods
Study area and data collection
Coliumo (36°30′S, 72°56′W, Fig. 1) is a shallow semiclosed north-facing bay with an approximate surface area
of 5 km2. Depths reach 25 m near the mouth and the sea
Mar Biol
Fig. 1 Coliumo Bay. Symbols
represent the sampling sites
per bathymetric stratum. Filled
circle: stratum 4 (>15 m), open
circle stratum 3 (15–10 m),
filled square stratum 2
(10–5 m), open square stratum
1 (<5 m), (filled diamond)
Marine Biology Station of the
University of Concepción at
Dichato
bed is mostly composed of sand, with a few rocky areas
in intertidal and subtidal zones. The sedimentary sea floor
is characterized mainly by coarse sand (>80 %), while
medium and fine sands are highly variable and spatially
heterogeneous (unpublished data). The sampling period
was spread over 12 cruises between October 2010 and July
2013 (October 2010; January, April, July, and October in
2011 and 2012; January, April, and July 2013). The months
of October, January, April, and July are representative of
the austral spring, summer, autumn, and winter seasonal
oceanographic conditions, respectively. During each cruise,
13 sites with one replicate each were sampled on board the
oceanographic vessel Kay–Kay II (University of Concepción, Chile). The sampling sites were defined according to
the bay’s bathymetry, selecting 3 sampling sites for each of
the following four bathymetric strata: 0–5 m (stratum 1),
5–10 m (stratum 2), 10–15 m (stratum 3), and >15 m (stratum 4). One additional site was incorporated in stratum 1
(Fig. 1).
Organisms were captured using a modified Agassiz trawl
(1 m wide × 1 m long × 30 cm high, lined with 5 mm
“knot to knot” netting) and transported live to the laboratories of the Marine Biology Station of the University of
Concepción located in the town of Dichato on the shore
of Coliumo Bay (Fig. 1). In brief, sampling consisted of
trawling the sea floor at a speed of 1.5–2 knots. Using a
GPS, the initial location (i.e., when the trawl touches the
sea floor) and the final location after a 5-min trawl were
both recorded. The average distance for the 156 trawls
conducted was 396 ± 87 m (mean ± standard deviation).
These were always conducted along the north–south axis
of the bay. The time period and trawl distance are justified
by the surface area and bathymetry of the bay (i.e., to avoid
overlapping of sampling sites and bathymetric strata), thus
minimizing the effect of capturing species with aggregate
spatial distributions. In the laboratory, each individual was
identified to species level or to the minimum possible taxonomic level and weighed (g) with an analytical balance
with 0.01 g sensitivity. Numbers and weights were standardized as ind. 500 m−2 and g 500 m−2, respectively, using
the relationship between the number of individuals and
area swept by the trawl at each sampling site (e.g., Nº ind.
X 500 m2/distance swept by trawl in m2). Trawl sampling
techniques have been used to describe and quantify epibenthic macrofaunal communities and demersal fish species in several environments (e.g. McKnight and Probert
1997; Callaway et al. 2007; Griffiths et al. 2008). Captured
organisms belonging to infaunal worms (i.e., polychaeta)
and other organisms <5 mm were extracted from the database and were not included in the analyses. At each sampling site, we characterized the hydrographic conditions of
the water column, using a CTDO sensor (model SD204)
to record temperature (°C), salinity, and dissolved oxygen
(mL L−1).
Analysis of aggregate and compositional community
variability
To assess the spatial and temporal variation of the epibenthic macrofaunal community in Coliumo Bay after 27F
(aggregate and compositional variability; Micheli et al.
1999), a two-way crossed design was used, with time and
bathymetry as factors. Time was taken as a fixed factor
with 12 levels (i.e., one sampling period for each level).
Bathymetry was a fixed factor with 4 levels (stratum 1–4).
Analyses were performed with PRIMER v6 and PERMANOVA+ for PRIMER (Clarke and Warwick 2001;
Clarke and Gorley 2006; Anderson et al. 2008). For indicators of community aggregate variability (i.e., univariate
data), the analyzed variables were as follows: species richness, Shannon-Wiener diversity index (α-diversity; Whittaker 1972), total community density, and total community
13
Mar Biol
biomass. For indicators of community compositional
variability (i.e., multivariate data), the entire community
(N = 156 samples and p = 72 taxa) was analyzed separately for species density and species biomass. For univariate data, analyses were performed on the raw data using
the Bray–Curtis dissimilarity measure. For multivariate data, analyses were conducted to assess the effect of
using different resemblance measures and different standardization/transformation of data (i.e., remove the effect of
dominant species; Anderson et al. 2006, 2011). The chosen
analyses were as follows: (i) BCR: Bray–Curtis dissimilarity measure with raw data (for density and biomass), (ii)
BCST: Bray–Curtis dissimilarity measure with standardized and fourth root transformed data (for density and biomass), and (iii) JDM: Jaccard dissimilarity measure with
presence–absence data. All these analyses exclude joint
absences. Probability values for main tests and pairwise
comparisons (when statistical differences were detected)
were obtained using 4,999 permutations of residuals under
a reduced model with sums of squares type III. Temporal
(intra- and inter-annual) and spatial (bathymetric) variation was represented graphically using non-metric multidimensional scaling (nMDS), performed with similar
resemblance measures and standardization/transformation
data above described. For the sake of simplicity, nMDS
was represented, separately, for temporal and spatial factors according to their estimated centroids. Finally, a set of
selected variables was superimposed using techniques of
proportional bubbles (Clarke and Warwick 2001; Anderson et al. 2008) on nMDS plots estimated using BCST
for density. Biological variables were as follows: species
richness, Shannon-Wiener index, total community density,
total community biomass, density and biomass of C. coronatus, Nassarius spp., Aphos porosus (toadfish), and the
total density and biomass of the 67 non-dominant species
of this community. Environmental variables were bottom
temperature, salinity, and dissolved oxygen. In the case
of environmental variables, the resemblance measure was
estimated from Euclidean distance based on normalized
data (EDN).
PERMDISP routines were conducted to test the homogeneity of multivariate dispersions for the several resemblance measures used. These analyses considered time and
bathymetry factors separately. Analyses were performed
with similar criteria using for PERMANOVA. PERMDISP
output was also used to assess whether the spatial structure
of the community was homogeneous throughout the bay
over time (i.e., between sampling periods and years). For
this analysis, the average dissimilarity was used as a multivariate dispersion indicator (i.e., β-diversity; Anderson
et al. 2006, 2011). Temporal decrease in this multivariate
indicator reveals spatial homogenization of the community
in Coliumo Bay and indicates community recovery.
13
Finally, in order to assess the changes in the community
over a longer timescale, from 3 years prior to 3 years following 27F, we constructed a comparative table including
both the hypoxia and the 27F event (i.e., pre-hypoxia, posthypoxia and years 1, 2, and 3 post 27F). The indicators of
community aggregate variability were species richness, the
Shannon-Wiener index, and total community density and
biomass. The indicators of community compositional variability were biomass and proportional density of C. coronatus, Nassarius spp., A. porosus and the total of non-dominant species of the community (Hernández-Miranda et al.
2012a). This analysis used information from January 2007
to July 2013 (27 sampling periods) from stations E1, E2,
and E3 (see Fig. 1). This qualitative analysis did not use
the same spatio-temporal methodology employed post 27F,
since the thirteen stations were only sampled from October
2010 onward.
Results
Community aggregate variability
From samples collected after the 27F event, a total of
44635 individuals were identified and measured, belonging
to 5 Phyla, 12 Classes, 31 Orders, 53 families, and 72 species (Table 1, Supplementary Material). The dominant species in terms of density were C. coronatus (44.8 %), Nassarius spp. (16.9 %), and A. porosus (4.7 %). The bivalve
Mulinia edulis made up 22.4 %, due mostly to two peaks
in January and April 2011. The dominant species in biomass were C. coronatus (79.6 %), Nassarius spp. (3.6 %),
and the flatfish Paralichthys adspersus (2.4 %). A. porosus
was in the sixth place with 1.2 %. There were significant
temporal differences in total community density (Table 1a),
with a tendency to decrease (Fig. 2a). The highest densities
were observed in January and April of 2011; these months
produced the majority of significant differences between
sampling periods (See Table 2, Supplementary Material for
pairwise comparisons). C. coronatus and the total of nondominant species (67 species) showed a similar density
pattern over time. Nassarius spp. showed high inter-annual
variability, with a strong tendency to decrease over time,
and the highest densities were generally recorded in October. The density of A. porosus increased over time, mainly
during the last year (Fig. 2a). Total community biomass
displayed significant differences over time (Table 1b), but
no inter-annual trends were detected (Fig. 2b). The highest values were observed in January 2012, which accounts
for most of the significant differences between sampling
periods (See Table 2, Supplementary Material for pairwise
comparisons). This pattern was strongly influenced by C.
coronatus. There was an important increase in the total
Mar Biol
Table 1 PERMANOVA output
for the indicators of community
aggregate variability
Source
df
SS
MS
Pseudo-F
P (perm)
Unique perms
(a) Total density
Bs
3
Sp
11
Bs × Sp
2,031.3
677.11
74,905
0.49362
0.8862
4,975
6,809.5
4.9643
0.0002
4,971
1.252
0.081
4,951
33
56,671
1,717.3
Res
104
142,660
1,371.7
Total
151
275,620
(b) Total biomass
Bs
3
Sp
11
Bs × Sp
4,324.4
31,137
1,441.5
0.89793
0.5074
4,985
2,830.7
1.7633
0.0144
4,974
1.0112
0.4584
4,953
33
53,570
1,623.3
Res
104
166,950
1,605.3
Total
151
258,360
(c) Species richness
Bs
3
5,529
Sp
11
8,488.7
Bs × Sp
5.0115
0.001
4,985
771.7
2.0984
0.0096
4,976
1.1569
0.2494
4,966
1,843
33
14,040
425.46
Res
104
38,246
367.75
Total
151
66,582
(d) Shannon-Wiener index
3
10,961
3,653.7
6.8857
0.0002
4,985
11
20,178
1,834.4
3.457
0.0002
4,979
1.4606
0.0244
4,966
Bs × Sp
Bs bathymetric stratum, Sp
sampling period. In bold, p
values <0.05
10000
Densitylog 10 (Ind. 500 m -2)
Bs
Sp
33
25,576
775.04
Res
104
55,185
530.62
Total
151
112,280
1000
a
1000
100
100
10
10
1
1
0.1
10000
Biomasslog 10 (g 500 m -2)
c
10000
b
d
1000
1000
100
10
100
1
0.1
10
0.01
1 1 1
0
3 3 3
2
2 2 2
1
01 01 01 01 01 01 01 01 01 01 01 01
t-2 n-2 r-2 l-2 t-2 n-2 r-2 l-2 t-2 n-2 r-2 l-2
Oc Ja Ap Ju Oc Ja Ap Ju Oc Ja Ap Ju
1
2
3
4
Bathymetricstratum
Time
Fig. 2 Spatio-temporal dynamics of epibenthic macrofaunal community at Coliumo Bay. a time series of density, b time series of biomass, c density for bathymetric stratum, and d biomass for bathym-
etric stratum. Filled circle total community, open circle C. coronatus,
open triangle Nassarius spp., inverted triangle A. porosus, and filled
square 67 other species
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Mar Biol
biomass of non-dominant species in April 2011, which
was maintained in subsequent sampling periods. Nassarius
spp. and A. porosus biomass displayed patterns similar to
those of their respective densities (Fig. 2b). Species richness varied significantly over time (Table 1c), but with no
trend at an inter-annual scale (Fig. 3a). In general, the values in spring and autumn were higher than those in summer and winter (for pairwise comparisons see Table 3, Supplementary Material). The Shannon-Wiener diversity index
was also significantly different over time, and was the only
indicator of community aggregate variability that displayed
a significant interaction with bathymetry (Table 1d). This
variable showed a sustained tendency to increase over time
(Fig. 3b), which was also observed in temporal comparisons of seasonal sampling periods (for pairwise comparisons see Table 3, Supplementary Material). The statistical
interaction found in the Shannon-Wiener diversity index
suggests that the continuous gradient, with increasing
diversity between shallower to deeper zones of Coliumo
Bay, was not found during all sampling periods. This may
be explained by the similar diversity found between bathymetries 2 and 3 (See Fig. 3d), which probably generated a
diversity transition area between the shallowest and deepest zones of the bay. The total community density did not
show significant differences among depths (Table 1a). C.
Species richness (S)
15
Community compositional variability
The PERMDISP analysis for community density revealed
significant dispersion differences among sampling periods
(i.e., time factor) for all resemblance analyses performed
(i.e., BCST: Pseudo-F11,140 = 2.3223, P (perm) = 0.024;
Fig. 4). BCST pairwise differences were found in 10 of
66 tests (15.2 %). In the case of bathymetry, no significant
12
a
c
11
10
10
9
8
7
5
1.8
Shannon-Wiener index (H’ )
coronatus and total density of non-dominant species tended
to decrease at greater depths. Nassarius spp. increased in
density at greater depths and A. porosus reached its highest density within the third bathymetric stratum (Fig. 2c).
Total biomass also showed no significant differences
among depths (Table 1b). As with density, the biomass of
C. coronatus tended to decrease at deeper depths and Nassarius spp. showed an inverse tendency. A. porosus had
greater biomass at greater depths, and the total biomass
of non-dominant species showed no differences between
bathymetric strata (Fig. 2d). Both species richness and the
Shannon-Wiener diversity index showed significant differences between depths (Table 1c, d, Fig. 3c, d). Both
indicators had a significant tendency to increase at greater
depths (See Table 4, Supplementary Material for pairwise
comparisons).
b
1.6
d
1.2
1.2
0.6
0.8
0.4
0.0
0 1 1 1
2 3 3 3
1
2 2 2
01 01 01 01 01 01 01 01 01 01 01 01
t-2 n-2 r-2 l-2 t-2 n-2 r-2 l-2 t-2 n-2 r-2 l-2
Oc Ja Ap Ju Oc Ja Ap Ju Oc Ja Ap Ju
1
2
3
4
Bathymetric stratum
Time
Fig. 3 Spatio-temporal dynamics of epibenthic macrofaunal diversity parameters (mean ± SE) in Coliumo Bay. Time series of species
richness (a) and Shannon-Wiener index (b). Species richness (c) and
13
Shannon-Wiener index (d) for bathymetric stratum. For a and b plots,
symbols correspond to spring (filled circle), summer (open circle),
autumn (filled triangle), and winter (open inverted triangle)
Mar Biol
Average dissimilarity (%)
55
45
35
25
1
2
3
0
1
2
2
1
3
1
2
3
01 01 01 01 01 01 01 01 01 01 01 01
t-2 an-2 pr-2 ul-2 ct-2 an-2 pr-2 ul-2 ct-2 an-2 pr-2 ul-2
J
J
J
A
O
A
O
A
J
J
J
Oc
Time
Fig. 4 Multivariate average dissimilarity (mean ± SE) for the epibenthic macrofaunal community obtained by PERMDISP analyses.
Percentages were estimated per sampling period. Symbols represent
different data analyses: (filled inverted triangle) Jaccard dissimilarity measure with presence–absence data, (filled circle) Bray–Curtis
dissimilarity measure with standardized and fourth root transformed
density data, and (open circle) Bray–Curtis dissimilarity measure
with standardized and fourth root transformed biomass data
dispersion differences were found for any of the analyses
performed (i.e., BCST: Pseudo-F3,148 = 1.1359, P (perm):
0.3826). The PERMDISP analysis found significant differences in dispersion of biomass over time (i.e., BCST:
Pseudo-F11,140 = 2.7781, P (perm): 0.012; Fig. 4), and for
BCST analyses, only 12 of 66 (18.2 %) of the pairwise
comparisons showed significant differences. As for density, there were no significant differences in dispersion of
the bathymetry factor for biomass (i.e., BCST: PseudoF3,148 = 1.909, P (perm): 0.1872). Density and biomass
differences detected over time are explained only by 2 or
3 sampling periods (for pairwise comparisons see Tables 5
and 6, Supplementary Material). The PERMDISP analyses of environmental variables from the sea floor (temperature, salinity, and dissolved oxygen) showed a similar
pattern to that of community density and biomass, with
significant dispersion values for the time factor (EDN:
Pseudo-F3,152 = 3.298, P (perm): 0.035), but without
significant differences for the bathymetry factor (EDN:
Pseudo-F3,152 = 1.8422, P (perm): 0.2082). For the time
factor, 23 of 66 pairwise comparisons (34.8 %) showed significant differences (for pairwise comparisons see Table 7,
Supplementary Material). These results, i.e., no significant
differences for the bathymetry factor (See Fig. 1, Supplementary Material) and only a small percentage of differences detected for the time factor across all analyses,
suggest that statistical inferences should focus mainly on
a location effect using PERMANOVA. Furthermore, a
decrease in average dissimilarity over time (β-diversity;
Fig. 4) is a clear signal of spatial community recovery in
Coliumo Bay.
The PERMANOVA analysis revealed a significant interaction between time and bathymetry for density (Table 2a),
as well as significant differences for the two factors separately. Similar results were obtained for each of the three
resemblance analyses (See Table 8, Supplementary Material). The community responses on intra- and inter-annual
timescales are clearly separated by the nMDS (Fig. 5).
Independent of the dissimilarity measure and the data transformation, for the three post 27F years studied, there were
intra-annual dynamics that began in spring (sampling periods 1, 5, and 9) and ended in winter (sampling periods 4,
8, and 12) and appeared to have a cyclical trend. This pattern is even more notable if the weights of more abundant
species are removed (See Fig. 2, Supplementary Material).
Furthermore, two inter-annual patterns stand out: The first
is the directional shift between samples of successive years,
beginning with one community structure in the first year
post 27F and changing to a different structure by the third
year (see the arrow direction in the estimated inter-annual
centroids; Fig. 5a). The second inter-annual pattern is the
differentiation between different seasons of each year. For
example, the summer sampling periods were segregated
from the winters in the 3 years following 27F (Fig. 5b). As
in the intra-annual dynamics, this pattern is more notable if
the weights of the most abundant species are removed (See
Fig. 2, Supplementary Material). Spatially, for all the resemblance measures utilized, there was a gradient of community density from the shallowest to the deepest bathymetries
(Fig. 5c). For biomass, the PERMANOVA analysis found
a significant interaction between time and bathymetry for
the estimates with BCST (Table 2b). The nMDS for time
and bathymetry showed patterns similar to those found for
community density (See Figs. 3, 4, Table 9, Supplementary Material). With slight differences, this temporal and
bathymetric pattern was also found for the environmental
variables on the bottom (Table 2c; Fig. 6. See also Table 10,
Supplementary Material). Temporally, the variables which
differentiated the community in the first year after 27F were
total community density, C. coronatus density, and Nassarius spp. biomass and density, while the variables that differentiated the community in the third year after 27F were
the A. porosus biomass and density, α-diversity (i.e., Shannon-Wiener index), and bottom dissolved oxygen (Fig. 7).
Bathymetrically, the variables which differentiated the community toward the deepest stratum were species richness,
α-diversity, and Nassarius spp. density and biomass, while
the variables which differentiated the community toward the
shallowest stratum were community density, density of C.
coronatus, total biomass of non-dominant species, and dissolved oxygen on the bottom (Fig. 8).
13
Mar Biol
Table 2 PERMANOVA output
for (a) compositional density
community, (b) compositional
biomass community, and (c)
bottom environmental water
column (temperature, salinity,
and dissolved oxygen)
Source
SS
df
MS
Pseudo-F
P (perm)
Unique perms
(a) Bray–Curtis standardized and fourth root transformed data
Bs
3
21,837
7,279
5.4758
0.0002
4,971
Sp
11
99,872
9,079.2
6.8301
0.0002
4,957
Bs × Sp
33
60,371
1,829.4
1.3762
0.0002
4,935
Res
104
138,250
1,329.3
Total
151
319,650
(b) Bray–Curtis standardized and fourth root transformed data
Bs
3
18,045
6,015
4.3524
0.0002
4,969
Sp
11
79,947
7,267.9
5.259
0.0002
4,945
Bs × Sp
33
58,448
1,771.1
1.2816
0.0024
4,944
Res
104
143,730
1,382
Total
151
301,460
(c) Euclidean distance based on normalized data
Bs bathymetric stratum, Sp
sampling period. In bold, p
values <0.05
Bs
3
25.264
8.4214
10.802
0.0002
4,990
Sp
11
312.04
28.367
36.388
0.0002
4,980
Bs × Sp
33
37.062
1.1231
0.0242
4,963
Res
104
84.196
0.77959
Total
151
465
27F and hypoxia context
The indicators of aggregate and compositional variability,
considering the periods defined as pre-hypoxia, post-hypoxia,
and years 1, 2, and 3 post 27F, are given in Table 3. Species
richness and the Shannon-Wiener index fell post-hypoxia,
and the latter recovered normal values by year 3 post 27F.
Total community density increased after hypoxia, decreasing
in the following 3 years after 27F. At the end of this period,
total community density decreased by one order of magnitude with respect to pre-hypoxia conditions. Total community
biomass was similar pre- and post-hypoxia, decreasing after
27F to almost one third of pre-hypoxia levels. Each species
was differentially affected by both perturbations. The density
and biomass of C. coronatus fell post hipoxia, but recovered
strongly in the first 2 years post 27F. However, only in year 3
post 27F was its proportional biomass greater than it was during pre-hypoxia. The Nassarius spp. increased both in density
and biomass post-hypoxia, but showed a strong and sustained
loss in the three post 27F years. The proportional density and
biomass of A. porosus and the non-dominant species of the
community fell post-hypoxia. However, following 27F, they
experienced a systematic recovery, with maximum values
recorded in year 3 post 27F.
Discussion
Community response after 27F
Earthquakes and tsunamis produce strong changes in
coastal areas, altering ecosystems directly and indirectly
13
1.4406
and changing their configuration in space and time. This
kind of disturbance may produce an abrupt resetting of the
existing conditions and an opportunity for the appearance
of new ecological dynamics (Holling 1973). The trajectory which these ecosystems adopt afterward will depend
mainly upon two factors: the speed of recovery of the
habitat, including its spatial heterogeneity; and the arrival
of new organisms capable of colonizing, surviving, and
reproducing in this new and altered environment (e.g., Halford and Perret 2009; Lomovasky et al. 2010). In physical
terms, for example, changes have been reported in the sedimentary structure and in the microfossil content of the sea
bed following the earthquake and tsunami in Japan in 2003
(Noda et al. 2007). Changes have also been observed in the
large amount of suspended sediment and the modifications
in the morphology of intertidal coastal zones in the northeast Indian Ocean following the tsunami that hit Sumatra
in 2004 (Yan and Tang 2008; Ranjan et al. 2010; Meilianda
et al. 2010). Biological changes were reported in the community of sea grass beds as a result of the tsunami in Thailand in 2004 (Whanpetch et al. 2010). An 8.0 earthquake
and tsunami in Peru in 2007 produced changes in the epibenthic faunal community of Paracas Bay, which affected
functional groups, whereby the increased abundance and
biomass of filter feeders also produced an increase in their
predators (Lomovasky et al. 2010). The uplift of the intertidal coastal zone off central Chile following a 7.8 earthquake in 1985 led to strong modifications of this marine
ecosystem, resulting in changes in species composition and
diversity and in the local biogeography (Castilla 1988).
In Coliumo Bay, the indicators of community aggregate variability displayed contrasting temporal dynamics,
Mar Biol
a
◂ Fig. 5 a, b Temporal nMDS plots for epibenthic macrofaunal density
10
6
11
7
2
9
5
8
3
1
12
4
b
Su3
Su2
A3
A2
Su1
Sp3
Sp2
W2
A1
Sp1
W3
W1
c
1
4
2
3
indicating that the responses after 27F were not the same
for all variables. Following a rapid increase, total density
decreased over time, indicating the negative inter-annual
effect of 27F. Total biomass and species richness revealed
no inter-annual trends or negative effects; however, both
indicators suggest strong intra-annual or seasonal dynamics. Only α- and β-diversity showed signals of recovery after 27F. There was an increase in α-diversity and a
decrease in β-diversity (See Figs. 3, 4). Despite these signs
analysis performed with the Bray–Curtis dissimilarity measure based
on standardized and fourth root transformed data (Stress = 0.09).
Numbers in panel a correspond to centroids estimated for each of the
12 sampling periods. Different lines connecting centroids (straight
line, doted and dashed lines) represent time series for each of the
three sampling years at an intra-annual scale. Arrows connect the centroids estimated for each of the three sampling years. In the panel b
the same estimated centroids are shown at an inter-annual timescale,
highlighting seasonal dynamics. Sp spring, Su summer, A autumn,
and W winter. Suffixes 1, 2, 3 correspond to each season for years 1,
2, and 3, respectively. Lines connect similar seasons among the three
sampling years. c nMDS plot obtained for bathymetric strata. Centroids for epibenthic macrofaunal density were estimated with Bray–
Curtis dissimilarity measure and data were standardized and fourth
root transformed. Suffixes correspond to each of the four bathymetric
strata. In this cases Stress < 0.01
of community recovery (according to α- and β-diversity),
total density and total biomass are still far below those
observed before the hypoxia and 27F events. Both total
density and total biomass are still ca. one order of magnitude below values reported by Hernández-Miranda et al.
(2012a) for 2007 (See also Table 3), when this bay had
not yet suffered the impact of any strong natural perturbation. The decrease in total community density and biomass is explained by the decrease in the dominant species
(C. corontaus and Nassarius spp.). Hernández-Miranda
et al. (2012a) discussed the ecological mechanisms of
short-term and medium-term community responses after
a strong natural hypoxic event occurred in January 2008.
They found that immediately after the hypoxia, which triggered a massive beaching and mortality of organisms, the
indicators of community aggregate variability (i.e., total
density, total biomass, and species richness) recovered rapidly (<3 months) to pre-perturbation values. In the medium
term, however (ca. 2 years), total density increased by an
order of magnitude, while total biomass maintained similar values. This rapid recovery of density also occurred
post 27F in the majority of community species. However,
after the strong increase in the first year, the trend in the
following 2 years was to decrease, mainly associated with
a systematic decrease in the density of Nassarius spp. Patterns of rapid recovery and later decrease in abundance
after strong disturbances have been described, for instance
by Lomovasky et al. (2010) for a macrobenthic community
(mainly infaunal) after a tsunami and by Halford and Perret (2009) for coral reef fish species after successive coral
spawn slick events.
From a compositional point of view, the community
displayed a variable structure after 27F. At an inter-annual
timescale, the community (both in density and biomass)
shifted through different structures with apparent directionality (see Fig. 5, Fig. 2 Supplementary Material). It is interesting to note that the community as a whole was different
during each of the 3 years post 27F. It is also interesting
13
Mar Biol
a
12
5
3
9
1
4
78
2
10
6
11
b
W3
Sp2
Sp3
Sp1
W1
W2
A1A2
Su1
A3
Su2
Su3
c
4
1
Resilience in Coliumo Bay
3
2
Fig. 6 a, b Temporal nMDS plots for bottom environmental variables (temperature, salinity and dissolved oxygen) (Stress = 0.02). c
nMDS plot obtained for bathymetric strata (Stress < 0.01). Centroids
were estimated from Euclidean distances based on normalized data.
Suffixes, numbers, symbols, arrows, and connecting lines as in Fig. 5
that this inter-annual differentiation displayed directionality or continuum, with no evidence of a return to the initial state observed immediately after 27F. These temporal
dynamics suggest that the community in Coliumo Bay
13
presents diverse compositional structures over time, which
allow it to maintain its ecological functions (i.e., Alternative Stable States, ASS; Beisner et al. 2003). Although
the direction the community will take in the future is an
open question, purely based on the observed inter-annual
dynamics, it seems that seasonal biological processes and
oceanographic conditions play an important role. As for the
aggregate variability indicators, the beginning of the reproductive period each year (i.e., spring recruitment), associated with seasonal oceanographic changes, could act cyclically, thus favoring the temporal stability of the community
(Figs. 5, 6). That is, spring of each year would be a new
starting point in the temporal community dynamics.
We also observed a spatial homogenization of the community over time (i.e., increase in α-diversity and decrease
in β-diversity). In other words, during each sampling
period, the sites occupied by each species increased with
respect to the previous period. We also detected a clear
community differentiation with respect to the bathymetry
factor (see Fig. 5c). A gradient between the deepest stratum
and the shallowest was observed in community density,
community biomass, and also in water column variables
(temperature, salinity, and dissolved oxygen), suggesting a spatial relationship between the community and the
hydrography of Coliumo Bay. Dissolved oxygen appears
to be the most important factor driving community spatial
differentiation. In fact, Hernández-Miranda et al. (2012a)
found that low dissolved oxygen conditions had a negative
effect on the aggregate and compositional structures of this
community. The observed pattern of lower total density and
biomass of the dominant species in the deepest zone (stratum 4, see Figs. 2, 8) is probably related to the presence
of very low dissolved oxygen concentrations. However, the
highest species richness and α-diversity of Coliumo Bay
were found in this zone, probably due to the fact that no
major hypoxia events (i.e., <0.5 mL O2 L−1) took place
during the 3 years following 27F.
The degree of stability and resilience of a community subjected to a mega-perturbation will determine whether it
does or does not maintain its structure and functionality
over time (Holling 1973; Peterson et al. 1998). These properties obviously emerge from responses at different spatial
and temporal scales (O’Neill 2001). Mega-perturbations
produce changes in environments, which can persist for
tens or hundreds of years (Nelson and Manley 1992; Turner
2010). Thus, the implications of such stochastic events are
of great relevance to ecosystem functioning. In ecological
community theory, a series of hypotheses have been proposed treating the role that species diversity plays in the
recovery of ecosystems following stochastic perturbation
Mar Biol
a
b
Su
Su
Su
A
A
W
Su
A
Su
Sp
Sp
W
d
Su
Su
A
W
Sp
Su
Su
Sp
A
A
W
Sp
W
f
Su
Su
W
W
Sp
Su
Sp
Su
A
A
A
W
W
Sp
Su
h
Su
A
A
W
Su
Sp
Sp
A
Sp
W
Su
A
Su
Sp
Sp
W
A
Sp
W
Su
A
Su
Sp
Sp
W
g
A
W
Su
A
Su
Sp
Sp
W
A
Sp
A
W
e
A
W
Su
A
Sp
Sp
W
W
c
Su
Sp
A
Sp
W
A
W
W
Sp
A
W
Fig. 7 Temporal nMDS plots for epibenthic macrofaunal density.
These plots correspond to analyses performed with the Bray–Curtis
dissimilarity measure based on standardized and fourth root transformed data (Stress = 0.09; i.e., Fig. 5a). Superimposed bubbles correspond to a total community density, b C. coronatus density, c Nas-
sarius spp. density, d Nassarius spp. biomass, e A. porosus density,
f A. porosus biomass, g Shannon-Wiener index, h bottom dissolved
oxygen. Black filled circle Year 1, (open circle) Year 2, (gray filled
circle) Year 3. Sp spring, Su summer, A autumn, W winter. Diameters
of bubbles are proportional to the magnitude of each variable
events, taking into consideration the periodicity and magnitude of such events. These include intermediate perturbations, dynamic equilibria, environmental heterogeneity, and
ecological time, among others (e.g., MacArthur and Wilson
1967; MacArthur 1972; Huston 1979, 1994; Castilla 1988).
In particular, the last two hypotheses may explain the
community dynamics of Coliumo Bay following 27F (i.e.,
more heterogeneous environments provide more niches and
thus greater species diversity; while the latter proposes that
the time which separates successive perturbations determines the increase in species diversity and the restructuring of the affected community). The strongly perturbed
13
Mar Biol
a
b
1
4
1
4
2
3
3
c
2
d
1
4
3
2
e
1
4
3
1
2
f
4
1
4
3
2
g
3
1
4
2
h
1
4
3
2
3
2
Fig. 8 Bathymetric nMDS plots for epibenthic macrofaunal density.
These plots correspond to analyses performed with the Bray–Curtis
dissimilarity measure based on standardized and fourth root transformed data (Stress < 0.01; i.e. Fig. 5c). Superimposed bubbles correspond to a species richness, b Shannon-Wiener index, c Nassarius
spp. density, d Nassarius spp. biomass, e total community density,
f C. coronatus density, g biomass of 67 other species, and h bottom
dissolved oxygen. Suffixes correspond to each of the four bathymetric strata. Diameters of bubbles are proportional to the magnitude of
each variable
Coliumo Bay displayed (1) a severe loss of organisms,
due to the initial mortality and homogenization of habitat
immediately after 27F, and (2) the arrival of organisms to
Coliumo Bay that allowed the recovery of the community
over time. These results also favor the idea that stability
and resilience are also linked to the ecological functionality
of species (Tilman et al. 1996; Peterson et al. 1998; Loreau
and Behera 1999; Walker et al. 1999; Elmqvist et al. 2003;
Hughes et al. 2005). In terms of the functional role of species in ensuring community resilience, Hernández-Miranda
13
Mar Biol
Table 3 Average and standard deviation values of the indicators of aggregate and compositional variability for the epibenthic macrofaunal community at Coliumo Bay
Period
Pre-hypoxia
2007
Aggregate
Species richness
11.91 ± 3.14
Shannon-Wiener index
1.2 ± 0.41
Total community density 1,562.33 ± 1,472
Total community biomass 5,467.16 ± 3,210.9
Compositional species density (%)
32.24 ± 29.41
C. coronatus
Nassarius spp.
A. porosus
Others 67 spp.
Species biomass (%)
C. coronatus
Nassarius spp.
A. porosus
Others 67 spp.
Number of samples
40.37 ± 40.33
10.31 ± 15.03
17.09 ± 18.99
44.32 ± 34.13
24.22 ± 34.29
2.6 ± 3.51
28.87 ± 28.48
11
Post-hypoxia
2008–2009
10.85 ± 3.24
1.1 ± 0.55
3,889.27 ± 5,609.2
5,596.7 ± 4,301.33
23.85 ± 29.04
55.66 ± 39.81
5.12 ± 7.77
15.38 ± 17.38
37.65 ± 33.87
34.86 ± 39.73
2.63 ± 6.25
24.86 ± 23.63
27
Year 1 post 27F
2010–2011
9.08 ± 2.57
1 ± 0.65
774.54 ± 1,270.18
2,176.21 ± 2,011.28
51.88 ± 38.45
19.49 ± 30.26
0.46 ± 1.39
28.16 ± 25.06
63.27 ± 40.79
11.42 ± 28.23
0.72 ± 2.16
24.59 ± 31.77
12
Year 2 post 27F
2011–2012
7.92 ± 3.23
1 ± 0.41
243.78 ± 222.24
4,221.86 ± 5,814.22
58.82 ± 27.94
19.57 ± 28.47
3.83 ± 5.09
17.79 ± 19.2
81.35 ± 22.68
4.32 ± 9.6
0.83 ± 1.14
13.5 ± 20.24
12
Year 3 post 27F
2012–2013
9 ± 3.74
1.26 ± 0.5
155.96 ± 115.8
1,858.96 ± 2,393.32
26.84 ± 21.54
10.16 ± 13.86
25.2 ± 29.85
37.8 ± 29.57
64.92 ± 37.92
1.36 ± 1.49
3.33 ± 4.69
30.39 ± 38.94
12
Comparative periods are related to two major perturbation events (January 3 2008 hypoxic event, and 27F mega-earthquake and tsunami).
For these comparisons, only sites E1, E2 and E3 were considered (See Fig. 1 and “Materials and Methods” section for details). Density: Ind.
500 m−2. Biomass: g 500 m−2
et al. (2012a) proposed that, in the short-term and mediumterm community, there are two underlying ecological
mechanisms in Coliumo Bay involved in the response
of the epibenthic macrofaunal community to the strong
natural perturbation: cross-scale resilience (Peterson et al.
1998) and response diversity (Elmqvist et al. 2003). In this
study, cross-scale resilience refers to (i) a high level of connectivity between Coliumo Bay and the adjacent coastal
areas favoring the rapid arrival (i.e., weeks) of organisms
from neighboring habitats of the continental shelf less
affected by the perturbation, which have very similar epibenthic macrofaunal communities in terms of composition
(Hernández-Miranda et al. 2009) and (ii) the differential
use of the habitat by the dominant species of the community. Response diversity, on the other hand, means that the
same ecological function could be performed by different
species of the community (Elmqvist et al. 2003). In the
case of Coliumo Bay, this function could be that of scavenger organisms.
Within the context of the cross-scale resilience hypothesis, our results indicate that after 27F, and independent of inter-annual trends, the greatest total community
density, total community biomass, species richness, and
α-diversity occurred mainly in spring and autumn (Figs. 2,
3). The recruits or juveniles that maintain these community attributes are the product of reproduction during the
winter–spring transition. They enter the bay at the end of
spring, and secondarily during autumn, from the shelf and/
or as the result of local reproduction within Coliumo Bay.
Spatial connectivity between Coliumo Bay and the adjacent
continental shelf could be determined by the synchronic
seasonal reproduction of many of the species of the community. Previous studies have indicated that maximum
reproductive activity for this coastal zone off central Chile
generally occurs at the end of winter and the beginning of
the austral spring (September) (Castro et al. 2000; Poulin
et al. 2002; Hernández-Miranda et al. 2003; Palma et al.
2006; Hernández-Miranda et al. 2009; Díaz-Cabrera et al.
2012; Veas et al. 2013). Mechanisms of cross-scale resilience may also be explained by the spatially different uses
of resources by species. It is interesting to examine the case
of C. coronatus and Nassarius spp., which are, in general,
the most abundant species in the community throughout
the entire study period. These scavenger species presented
segregated patterns of spatial distribution (see Figs. 2, 8)
suggesting a differential use of the food resources they
potentially compete for. While C. coronatus preferably
uses the shallowest zones of the bay, Nassarius spp. inhabits deeper areas. Also, the difference in body size suggests
that displacement capacity is much greater in C. coronatus,
which also decreases the possibility of competitive interference between these two species. The second ecological
13
Mar Biol
mechanism for explaining the maintenance of the community in Coliumo Bay is the Response Diversity Hypothesis,
also known as functional redundancy (Walker et al. 1999).
The scavengers C. coronatus and Nassarius spp. belong to
the same functional group, although they display opposite
responses to 27F. Compared to the densities and biomass
reported by Hernández-Miranda et al. (2012a), C. coronatus increased proportionally after 27F, while Nassarius spp.
suffered a drastic decrease (see also Table 3). Both species
fulfill the fundamental role of re-incorporating organic matter into the ecosystem, thus favoring the recovery of ecological functions carried out by the community and biogeochemical functions of the ecosystem. The recovery of
systems impacted by large perturbations has been attributed
not only to an increase in the diversity of isolated species,
but also to an increase in the diversity of functional groups,
since species which perform similar ecosystem functions
may operate at different scales and thus increase the rate of
recovery (Tilman et al. 1996; Peterson et al. 1998).
Finally, within the context of two major perturbations
that struck Coliumo Bay in the last 6 years (hypoxia and
27F), some similarity in compositional structure can be
seen mainly due to the presence of dominant species.
Although 27F generated a decrease in dominant species,
compositional structure was still generally dominated by
C. coronatus, Nassarius spp, and A. porosus. These species grouped together changed on average from 82.3 to
62.2 % in density and from 71.1 to 69.6 % in biomass
between the pre-hypoxic period and the third year after
27F. The non-dominant species increased in density from
17.09 to 37.8 % and from 28.87 to 30.39 % in biomass
during this period. For the pre- and post-hypoxia community, the analysis of community similarity showed that
the species responsible for the temporal dynamics in total
abundance and total biomass were C. coronatus, Nassarius
spp., and A. porosus (Hernández-Miranda et al. 2012a, b).
Following two major perturbations, the most affected species in the community remain the dominant species. This
pattern of alternate dominance suggests a certain degree of
long-term compositional macro-stability in this community. Beisner et al. (2003) proposed that the global stability of a community will be determined by the presence of
different ASS, which given certain basic characteristics of
functionality may be sustained over time. The inter-annual
community dynamics observed in Coliumo Bay suggest
that ASS are able to be developed by this community over
time, and the roles of several species of this community are
interchangeable. The response of the epibenthic macrofaunal community of Coliumo Bay after 27F, with an overall
structure that was directionally modified over time, suggests the presence of ASS sustained under two functional
underlying ecological mechanisms: cross-scale resilience
and response diversity.
13
Acknowledgments This study was funded by FONDECYT
11100334 and 1130868 to E. Hernández-Miranda and by the Programa de Investigación Marina de Excelencia (PIMEX) of the Faculty
of Natural and Oceanographic Sciences (University of Concepción,
Chile). J. Cisterna was funded by a scholarship from CONICYT (Beca
Magister 2010–2012) and by FONDECYT 11100334. R. A. Quiñones
and E. Hernández-Miranda received additional funding from the Interdisciplinary Center for Aquaculture Research (INCAR; FONDAP Project Nº15110027). The authors would like to thank three anonymous
reviewers and the Associated Editor Dr. M. G. Chapman for their valuable comments and suggestions to improve the quality of the paper.
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