Estuarine, Coastal and Shelf Science 60 (2004) 49e57
www.elsevier.com/locate/ECSS
Scales of variability in the sediment chlorophyll content
of the shallow Palmones River Estuary, Spain
S. Moreno), F.X. Niell
Department of Ecology, Faculty of Science, Campus Universitario de Teatinos S/N, University of Málaga, 29071-Málaga, Spain
Received 6 June 2003; accepted 28 November 2003
Abstract
A study on the spatial distribution of chlorophyll pigments (CP) at different scales in the sediments of the Palmones River
Estuary was carried out. Intertidal and subtidal sediments were sampled across a range of spatial scales: centimetres (depth and
replicate samples), meters (left and right banks, middle of the estuary) and kilometres (mouth to upper part of the estuary). CP
concentration was in the same order of magnitude as in the other estuarine areas, and followed a similar distribution. Important
spatial variation occurred at a broad scale (between stations, km), while, the scale in the order of centimetres was comparatively less
important. Because the variability in the CP distribution was dependent upon scale, a ratio between the CP variation at different
scales is proposed. This ratio showed that the changes that occurred in depth were much more important than those occurring in the
longitudinal axis of the estuary. This was due to the strong gradient found for chlorophyll in depth. Different biotic and abiotic
factors determine the spatial distribution. Differences between the stations are mainly related to hydrodynamic forces (waves, winds
and tides). Light penetration through the water column and into the sediment surface can explain differences in depth, and between
subtidal and intertidal sediments.
Ó 2004 Elsevier Ltd. All rights reserved.
Keywords: chlorophyll pigments in sediment; spatial variability; Palmones River Estuary
1. Introduction
Two fundamental and interconnected concepts in
ecology are the distribution pattern of variables and
their scale. These two concepts are among the central
topics in ecological studies (Levin, 1992). The description of the distribution pattern is the description
of variation in space, and the quantification of this
variation requires a reference to the scale. Thus, the
identification of variation is an entrée into the identification of scales (Denman and Powell, 1984; Powell,
1989).
There is no single natural scale at which ecological
systems should be studied. Systems generally show
a wide variability of spatial and temporal range and
organisation scales. Organisms show spatial and temporal patterns of distribution that depend on the
) Corresponding author.
E-mail address: [email protected] (S. Moreno).
0272-7714/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2003.06.006
observation scale. Benthic microalgae, expressed as the
main origin of the total chlorophyll a in the sediment
(Brotas and Plante-Cuny, 1996), is quite an interesting
topic to study because they present heterogeneity scales
in space as well as in time; the study of these scales has
been subject to some mathematical approaches (Shaffer
and Onuf, 1985; Plante et al., 1986; Shaffer and Cahoon,
1987). Different abiotic (e.g. light, sediment type and
tidal height) and biotic variables (e.g. bioturbation and
grazing) operate at different scales to determine spatial
distribution (Brotas and Plante-Cuny, 1996; McIntyre
et al., 1996; Cahoon et al., 1999). Most recent articles try
to recognise the main biotic and abiotic variables that
affect the spatial and seasonal distribution of the
microphytic populations in intertidal systems, although
no attempt has been made to examine how the
variability changes with the scale of description.
The aims of this study are the characterisation of the
spatial variability of chlorophyll pigments (CP) at
different scales (km, m and cm) trying to identify the
main factors that influence the observed variations, and
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S. Moreno, F.X. Niell / Estuarine, Coastal and Shelf Science 60 (2004) 49e57
to define an index to standardise this variability in the
Palmones River Estuary. The estuary is a well studied
area from a biogeochemical point of view (e.g. Clavero
et al., 1991, 1992, 1994, 1997a,b, 1999a,b, 2000; Estacio
et al., 1999; Avilés et al., 2000), but there have not been
previous studies dealing with the chlorophyll content in
the sediment and its spatial heterogeneity.
2. Material and methods
2.1. Study area
The Palmones River Estuary is located in Algeciras
Bay (southern Spain) at the end of a small catchment
area (302 km2). Palmones is a well mixed shallow
estuary with a maximum depth of 3.5 m and a range
of salinity from 29 to 35 (Clavero et al., 1997a). Tidal
movements have a maximum amplitude of 2 m, and
extensive areas of mud emerge daily at low tide (Clavero
et al., 1997a).
The estuary is under the influence of important
anthropogenic activities (physical and industrial origin).
The main perturbation has arisen since the construction
of a dam which started to store water in 1987 with
changes related to the reduction of the river water flow
between the dam and the estuary (Clavero et al., 1997a,
1999b).
2.2. Sampling and analytical methods
A total of 81 cores of sediment were collected in
December 2001 to examine the spatial variation in the
distribution of CP in the sediment. Samples were
collected at low tide in three representative stations
located in the main longitudinal axis of the estuarine
river (station 1, St. 1, at the mouth of the estuary, St. 2
at 3 km from St. 1 and St. 3 at 5 km from the mouth,
Fig. 1). At each station three sites were chosen: the left
(L) and right side (R) in the estuarine intertidal (130 m)
and the central (C) submerged position (subtidal) following a transversal transect.
At each site, nine contiguous cores were taken within
a square of 25 ! 25 cm. They were divided into a superficial (0e4 cm) and a deeper sample (6e10 cm) to extract
the pigments. This division was made considering the
maximum bacterial concentration at 6 cm as reported by
Clavero et al. (1999a).
PVC core tubes (4.5 cm i.d., 20 cm long) were
inserted by hand into the sediment, closed with a silicon
stopper and carefully transported in a vertical position
to the laboratory in an icebox at 4 (C.
CP were extracted in 80% acetone for 24 h in
darkness at 4 (C and were determined spectrophotometrically following the method of Lorenzen and Jeffrey
(1980). The results are expressed in mg chorophyll
pigments g1 sediment dry weight (mg g1dw). The
acetone extract includes several substances, including
chlorophyll a and pheopigments.
Organic matter was measured in each segment as
a percentage of weight loss by ignition (550 (C, 4 h)
from the 60 (C dried sediment.
Total particulate carbon and nitrogen were determined in surface and deeper layer with a CHN Perkin
Elmer Elemental Analyser following the method used by
Kristiensen and Andersen (1987).
Granulometric analyses of sediments were carried out
by a combination of dry and wet sieving (grain size
categories: O2000 mm for break-stone, 1000, 500, 250,
150 and 63 mm for different sizes of sand). The fine
fraction (!63 mm, silt and clay) was further separated
gravimetrically.
2.3. Statistical analysis
Graphical assessment of normality, as described in
Zar (1984), showed a normal distribution of data.
A two-way ANOVA was used to examine the effects
of depth (0e4 cm and 6e10 cm) and replicate samples of
spatial variation in the distribution of total CP in the
sediment in each sampling point (L1, C1, R1, L2, C2,
R2, L3, C3 and R3). A two-way ANOVA was used in
each station in order to compare the differences between
depths and localities (L, C and R). In order to compare
the differences between stations (1, 2 and 3), a three-way
ANOVA was made considering the factors of depth,
localities and stations. Finally a four-way factorial
ANOVA was necessary to calculate the contribution
of each factor (depth, replicate samples, localities and
stations) to the total variance of chlorophyll concentration in the sediment. It was calculated as described in
Sokal and Rohlf (1995).
In all the cases, the significance level was of 5%
(a ¼ 0:05). It was used in the model I ANOVA (depth,
replicate samples, localities and stations were considered
a fixed factor instead of random factor as in model II
ANOVA).
All the ANOVAs were model I and the null
hypothesis was rejected at the 5% significance level.
Multiple post hoc comparisons among means were
tested by Fisher’s LSD test (Sokal and Rohlf, 1995).
2.4. Variability index
The variability index described in this study is defined
as the relationship between mean squares (MS, obtained
in the four-way ANOVA) and the scale. This index is
expressed in units of variability per meter (uv m1). This
ratio is a standardisation of the variability to the scale and
S. Moreno, F.X. Niell / Estuarine, Coastal and Shelf Science 60 (2004) 49e57
51
Fig. 1. Map of the Palmones River Estuary showing location of sampling stations (1, 2 and 3: number of station, L: left bank, C: middle of estuary
and R: right bank).
allows us to compare the chlorophyll content between and
within ecological systems at different scales.
3. Results
3.1. Sediment characterisation
The average content of total organic matter of dry
sediment ranged from 0.3 to 6.4% (Fig. 2). In general,
the highest values were found in St. 2 and 3, whereas the
lowest ones were found in St. 1 and the centre of the
channel. Despite the differences in organic matter
content, they were not significantly different.
The C:N ratio ranged from 11.4 to 59.3 (Fig. 3). The
values were lower in St. 2 and 3 than in St. 1 and no
significant differences were revealed, comparing the
mouth of the river and the other stations.
The surface sediments of the Palmones River Estuary
are usually sandy (Fig. 4). The percentage of sand varied
from 61 to 99%. Sand is found at the mouth (St. 1) and
sandy-mud in the other inner stations of the estuary
(St. 2 and 3). There was an increase in the fine fraction
towards St. 3. In general, this fraction (!63 mm) is
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S. Moreno, F.X. Niell / Estuarine, Coastal and Shelf Science 60 (2004) 49e57
Fig. 2. Mean content of total organic matter in depth at the three sampled stations (St. 1, St. 2, St. 3).
mainly constituted of silts (0.1e37%). The clay minerals
ranged from 0.7 to 10%.
3.1.1. Distribution of chlorophyll pigments in
the sediment and ratio of chlorophyll
to total organic matter
The concentrations of CP in the sediments of each station at different depths are shown in Fig. 5. An increase
in concentration was observed from the mouth of the
estuary (St. 1, values lower than 2 mg g1dw) to stations 2
and 3 (concentrations ranging from 6.13 to 15.19 mg g1dw
in surface layer and from 0.52 to 3.87 mg g1dw in deeper
layer at St. 2; from 2.24 to 14.46 mg g1dw in surface layer
and from 0.35 to 5.98 mg g1dw in deeper layer at St. 3).
Three-way ANOVA results showed significant differences
between CP content at different stations (Table 1).
Stations 2 and 3 showed a similar trend in the distribution of the CP at different localities (L, C and R),
which differed from St. 1. In the inner stations (St. 2 and
3), the concentrations were higher on the left bank and
lower in the centre of the channel, around 2.5 (St. 2) to
6.5 (St. 3) times higher on the surface layer, and 7.4 (St. 2)
to 17 (St. 3) times higher in deeper layers. The results were
analysed using a two-way ANOVA that showed significant differences between the localities (Table 2).
The content of CP was much higher in the upper
sediment layer than in deeper ones (approximately 10
times). Only at St. 1 (left bank) some replicate samples
showed higher concentrations in deeper layers.
The typical deviations shown in Fig. 5 are indicative
of the heterogeneity between replicate samples.
A two-way ANOVA used to examine the effects of
depth and replicate samples in each sampling point (L1,
C1, R1, L2, C2, R2, L3, C3 and R3) indicated that the
differences in depth are significant. In the majority of the
replicate samples, there were significant differences
(Table 3).
The ratio of chlorophyll pigments to organic matter
can be used as an index of sediment quality, low values
correspond to low photo-autotrophic capacity relative
to total organic matter. This ratio ranged from 0.004 to
0.2 (mg g1) (Fig. 6). This ratio showed lower values in
St. 1 and in the centre of the channel. Differences in
depth were only found at St. 2, being approximately 10
times less in deeper layers than in surface sediments.
Fig. 3. The C:N ratio in depth at the three sampled stations (St. 1, St. 2, St. 3).
S. Moreno, F.X. Niell / Estuarine, Coastal and Shelf Science 60 (2004) 49e57
53
Fig. 4. Differences in the grain size distribution between stations (L, left bank; C, centre course; R, right bank).
3.1.2. Variation in chlorophyll pigments distribution
at different spatial scales
Four-way ANOVA revealed that CP distribution
varied across the various spatial scales examined in the
Palmones River Estuary (depth and replicate samples in
the range of cm, localities of m and station of km)
(Table 4). Most of the variation in the distribution of the
CP at different spatial scales in the sediment was due to
interactions (first, second and third order), almost 70%
of the total variation, while the error term only
accounted for 0.10%. The lower value of the error term
is indicative of the higher prediction power of the
analysis. The spatial distribution at small scale explained
9% of total variation (depth 8% and replicate samples
!1%) while the variation attributable to the spatial
distribution at large scale was 22% (stations 13% and
localities 9%).
However, the variability index (uv m1) indicated
that the most important scales of spatial variation occur
in scale of centimetres (depth), while the variation at
large scale (localities and stations) appears not to be so
important (Table 5).
4. Discussion
The estuarine sediment composition is dominated by
tidal influence; an increase in the accumulation of organic
materials has been observed for 10 years, showing high
progressive eutrophication (Carreira et al., 1995; Niell
et al., 1996; Clavero et al., 1997a, 1999b, 2000). This can
be associated with a high productivity, organic matter
accumulation from industrial and urban waste as well as
agricultural run-off, together with slow flow from the
reservoir. Several studies have shown that the organic
matter content in the sediment decreases with depth
(Dauer et al., 1987; McComb et al., 1998; Galois et al.,
2000; Jorcin, 2000). In Palmones, there are some studies
that show a discontinuity in deeper layers because of the
bacterial abundance at 6 cm (Clavero et al., 1999a, 2000);
nevertheless, the absence of a clear trend with depth was
observed in this study. Many authors have explained that
this fact is the result of two main factors: the rain and the
sediment reworking by bioturbation and erosion/resuspension processes (Anderson, 1983; Grant and Daborn,
1994; Galois et al., 2000).
Fig. 5. Mean concentration of chlorophyll pigments content in depth at the three sampled stations (St. 1, St. 2, St. 3).
54
S. Moreno, F.X. Niell / Estuarine, Coastal and Shelf Science 60 (2004) 49e57
Table 1
ANOVA table for the distribution of chlorophyll pigments (CP) in the
sediment in order to compare the differences between stations (St. 1, 2
and 3) (* significant for significance level 5%)
Source of variation
df
F
Station
Localities
Depth
Station ! Localities
Station ! Depth
Localities ! Depth
Station ! Localities ! Depth
Error
2
2
1
4
2
2
4
158
52.60*
44.54*
99.27*
15.15*
28.55*
7.02*
2.44*
Differences in the granulometric analysis of sediment
were found. At St. 1 sandy texture differs from sandymud texture in the upper part of the estuary. In general,
the mouths of rivers receive materials from the bay and
the river (mainly sand). These sites are exposed to
hydrodynamic processes (tide, wind, waves, etc.) that
avoid the deposition of fine fractions as clay (Coljin and
Dijkema, 1981). Estacio et al. (1999) observed that
accumulation of organic matter decreases when clay
content is low. A previous study in the Palmones
indicated that the main mineralogical compound is
quartz (Avilés, pers. comm.).
The C:N ratio did not show differences between the
surface and deeper layers (0e4 cm versus 6e10 cm
depth). The higher values of the C:N ratio in St. 1 suggest a high inorganic carbon content (mainly carbonate
shell fragments, as visual observations supported) since
organic matter and pigment content were very low,
while the C:N values in the inside stations can be related
to a highly degraded allochthonous organic matter.
Niell (1980) used the chlorophyll pigments/organic
matter ratio (mg g1) as an index of the sediment quality
in the NW estuaries of Spain, suggesting that higher
values (1e2) are an indication of good sediment quality
(e.g. sediments not affected by pollution) while the lower
values (!1) are associated with poor sediment quality.
Comparing the obtained ratios with those of similar
estuaries in Spain indicated by other authors (Table 6) it
could be concluded that the sediments of the Palmones
River Estuary are of low quality, the organic matter is
refractory, not very productive and of allochthonous
origin.
Table 2
ANOVA table for the distribution of chlorophyll pigments (CP) in the
sediment in order to compare the differences between localities (L, C
and R) in each station (* significant for significance level 5%)
Source of variation
Depth
Localities
Depth ! Localities
Error
Station 1
Station 2
Station 3
df
F
df
F
df
F
1
2
2
54
1.77
46.73*
4.63*
1
2
2
54
158.26*
33.28*
6.49*
1
2
2
54
17.88*
23.28*
3.31*
Table 3
ANOVA table for the distribution of chlorophyll pigments (CP) in the
sediment in order to examine the effects of depth (0e4 cm and
6e10 cm) and replicate samples in the sediment in each sampling point
(L1, C1, R1, L2, C2, R2, L3, C3 and R3) (* significant for significance
level 5%)
Localities Source of
variation
Station 1
Station 2
Station 3
df F
df F
df F
Left bank
Depth
Sample
Depth !
Replicate sample
1
7
7
Error
16
Center course
Depth
Sample
Depth !
Replicate sample
1
2
2
Error
Right bank
Depth
Sample
Depth !
Replicate sample
Error
21.90*
17.20*
15.95*
1 3705.7*
8
53.10*
8
34.93*
18
47.49*
11.85*
5.26*
1
8
8
212.34*
12.52*
18.92*
18
1 8492.43*
2 1756.34*
2 1319.94*
1
2
2
6
6
6
1 273.19*
2 254.06*
2 49.69*
1
2
2
6
6
202.54*
1.12
1.28
366.70*
291.28*
340.09*
1 1086*
2
0.62
2 209.16*
6
CP, mainly chlorophyll a, in the sediment is a key
variable for the study of the productivity of estuarine
systems. The CP values present a similar range to other
temperate intertidal ecosystems (Shaffer and Onuf, 1985;
Brotas and Plante-Cuny, 1996), as well as the spatial
distribution: the differences between the mouth and the
inside stations (De Jong and De Jonge, 1995), and the
decrease with depth (Cadée and Hegeman, 1977; Cadée,
1980; De Jonge and Coljin, 1994; De Jong et al., 1994).
The spatial distribution of CP in the sediment
depends on the scale of description (Stommel, 1963;
Haury et al., 1978). Furthermore, there is not a single
natural scale at which ecological processes can be
studied. For this, the first step was to determine at
which scale variability happened.
This study shows evidence that the spatial distribution of CP is very heterogeneous. This spatial heterogeneity is significant at the smallest and the greatest
spatial scale examined. In Palmones, the chlorophyll is
patchy at a range of spatial scales from centimetres to
kilometres. The most important spatial variation occurs
at a broad scale (stations and localities), while the
spatial variation at the centimetre scale (between
replicate samples and depth) seems to be less important.
The spatial variation between replicate samples is
comparatively unimportant compared with the other
sources of variance. Several authors have found the
same pattern in other similar marine systems (Sundbäck,
1984; Light and Beardall, 1998).
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S. Moreno, F.X. Niell / Estuarine, Coastal and Shelf Science 60 (2004) 49e57
Fig. 6. The ratio of chlorophyll pigments/organic matter (mg g1) in depth at three sampled stations (St. 1, St. 2, St. 3).
Given that variability is dependent on scale, a variability index is proposed in this study to solve this
problem. The index considers the scale and allows
comparison of the chlorophyll concentration between
and within ecological systems at different scales. The
obtained values of this index show that the changes that
occur in depth are much more important than those
occurring at a broad scale and between replicate
samples. This result is due to the strong gradient in
depth.
Different biotic and abiotic factors operating at
different scales affect the spatial distribution of CP in
Table 4
Analysis of variation in the spatial distribution of chlorophyll
pigments (CP) (* significant for significance level 5%)
Source of variation
df
MS
F
%
the sediment. The large differences in chlorophyll levels
between the mouth and St. 2 and 3 may be ascribed to
differences in hydrodynamic energy (waves, wind and
main tide). Generally, the mouth of a river undergoes
more turbulent hydrodynamic conditions, where the
average biomass and chlorophyll and clay content are
low. This is in agreement with the results of Coljin and
Dijkema (1981), who have reported that the chlorophyll
a is negatively correlated with hydrodynamic energy and
positively with clay content.
The light availability at the sediment surface is
affected by variability in water characteristics. Avilés
(pers. comm.) detected in the water column in the
Palmones a maximum value of total suspended solids of
340 mg l1, a possible explanation for the low CP
concentration in subtidal sediments; as a result, the CP
concentrations are higher in intertidal sediments.
The decrease in CP with increasing sediment depth in
Palmones is explained by the light penetration to
a maximum depth of 2e3 mm in the sediment (Coljin,
1982; McIntyre et al., 1996). Generally about 25% of the
biomass present in the 0e10 cm layer can be found in
the layer of 0e1 cm (Cadée and Hegeman, 1974; De
Jonge and Coljin, 1994; De Jong et al., 1994). Although
active migration by benthic microalgae (Cadée and
Hegeman, 1974; Pinckney et al., 1994) and bioturbation
(Cadée, 1976) has been demonstrated in intertidal
sediments, sediment reworking by hydrodynamic energy
(De Jong and De Jonge, 1995) is a more plausible
Main effects
Replicate samples
Depth
Localities
Station
2
1
2
2
3.34
590.62
220.83
314.86
12.04*
2131.80*
797.08*
1136.46*
0.13
8.19
9.18
13.09
Two factor interactions
Station ! Replicate samples
Station ! Depth
Station ! Localities
Location ! Depth
Location ! Replicate samples
Replicate samples ! Depth
4
2
4
2
4
2
3.91
169.91
70.71
35.89
3.32
4.38
14.10*
613.27*
253.27*
129.53*
11.99*
15.80*
0.91
14.12
17.44
2.96
0.76
0.68
4
1.60
5.78*
0.66
8
6.16
22.25*
8.81
Table 5
Variability index of chlorophyll pigments (CP) in the sediment of
Palmones River Estuary
4
4
11.70
7.83
42.22*
28.26*
5.70
3.77
Scale of variability
Variability index
(units of variability
per meter)
8
4.79
17.29*
13.51
54
0.28
Depth
Replicate samples (small)
Localities (transversal axis)
Station (longitudinal axis)
5906.2
27.83
1.7
0.1
Three factor interactions
Localities ! Replicate
samples ! Depth
Station ! Localities !
Replicate samples
Station ! Localities ! Depth
Station ! Replicate
samples ! Depth
Four factor interaction
Station ! Localities !
Replicate samples ! Depth
Error
0.10
56
S. Moreno, F.X. Niell / Estuarine, Coastal and Shelf Science 60 (2004) 49e57
Table 6
The ratio of chlorophyll pigments (CP) to organic matter in other
temperate intertidal ecosystems
Localities
Chlorophyll
pigments/organic
matter (mg g1)
Reference
Areiño, Rı́a Vigo
1.9
Foz del Miñor,
Rı́a Vigo
Placeres, Pontevedra
300 m from wwtpa
100 m from wwtp
Palmones,
Algeciras Bay
St. 1
St. 2
St. 3
0.2e1.9
Figueras (1956),
Margalef (1958)
Anadón
(pers. comm.)
Niell (1980)
a
1.1e1.8
0.2
This study
0.004
0.1
0.07
Waste water treatment plant.
explanation for higher values of CP in the deeper layer
in St. 1 than in the surface layer.
Acknowledgements
This work has been supported by the AMB99-1088
and REN2002-00340 projects of the Spanish Commission Interministry of Science and Technology. Thanks
to laboratory colleagues for their collaboration in
sampling, specially to Vicente Clavero, professor of
Ecology in Málaga University, who was involved in
biogeochemical research in the Palmones River from the
1980s until his death in August 2002.
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