Water management and climate changes increases the phosphorus ...

Abstract
Ž .
The Science of the Total Environment 228 1999 193202
Water management and climate changes increases the
phosphorus accumulation in the small shallow estuary
of the Palmones River ž southern Spain/
´
Vicente Claveroa, , Juan Jose Izquierdoa , Laura Palomoa ,
J. Antonio Fernandezb , F. Xavier Niella ´
a
Departamento de Ecologia Uniersidad de Malaga, ´ Facultad de Ciencias, Campus de Teatinos, Malaga 29071, Spain
b
Departamento de Biologia Vegetal. Uniersidad de Malaga, ´ Facultad de Ciencias, Campus de Teatinos, Malaga 29071,
Spain
Received 18 November 1998; accepted 2 February 1999
To estimate the potential contribution of sediment bound phosphorus to the enhancement of production in a small
shallow estuary Ž Palmones River. different fractions of sediment bound phosphorus were measured during two time
periods Ž 19871989 and 19931995 . . Following the first time period, construction of a dam decreased the discharge
from the Palmones River catchment, while climate changes resulted in a severe drought which further decreased
power discharge. The results show important biological and chemical changes in the sediment: during the latter time
period net accumulation of 157 g P m 2 year1 , while the rate during the earlier period was 1.18 g P m2 year1 .
1999 Elsevier Science B.V. All rights reserved.
Keywords: Sediment; Phosphorus; Estuary; Climate changes
1. Introduction
Estuaries are among the most eutrophic environments
on Earth Ž Nixon et al., 1986 . . When
organic matter is accumulated due to high productivity,
their sediment may act as a phosphorus
sink and phosphorus could be liberated in a re-
Corresponding author. Tel: 34-95-2131844; fax: 34-95-
2132000; e-mail: vic@uma.es
0048-969799$ - see front matter 1999 Elsevier Science B.V. All rights reserved.
Ž .
PII: S 0 0 4 8 - 9 6 9 7 9 9 0 0 0 4 5 - 5
duced environment from sediment to the water
enhancing production in an amplified positive
feedback ŽVan
Cappellen and Gaillard, 1996;
Furrer et al., 1996 . . An increase in the total
phosphorus content at the upper part of the sediment
would be an index of progressive eutrophication
in subarid areas of southern Spain
Ž Fernandez, ´ 1986; Clavero, 1992. where the P
cycling has been well studied ŽPerez-Llorens
´
and
Niell, 1990; Clavero et al., 1991, 1992, 1997a,b;
Hernandez, ´ 1992; Carreira et al., 1995; Izquierdo,

194
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V. Claero et al. The Science of the Total Enironment 228 1999 193202
1996 . . Water management is a paramount problem
in subarid countries, and the construction of
water reservoirs is a frequent management tool.
In the early 1980s a dam was built in the upper
part of the Palmones River which started to store
water in 1987. The normal rainfall in the catchment
area Ž averaged for the last 30 years. ranged
from 800 to 1050 mm year1 , however, in the last
3 years Ž 19931995. there has been a persistent
1 drought, 718 mm year Ž Carreira et al., 1995 . .
As a consequence of both situations two main
transformations in the catchment area of the
Palmones River have occurred in recent years: Ž. 1
the reduction of the river discharge by the construction
of the dam in its upper part and Ž. 2
climatic changes which led to a severe drought
which affected the flow of water in the river
between the dam and the estuary. The water flow
decreased in the estuary from 8 m 3 s 1 in 1987 to
3 1 Ž .
4 m s in 1995 Carreira et al., 1995 . Simultaneously
the input of phosphorus increased as a
consequence and an increase in the levels of total
phosphorus in the sediment should have been
expected over the same period. The decrease of
freshwater input changed the tidal exchange and
the input of phosphate by tidal flux also contributes
to increased eutrophication ŽClavero
et
al., 1997a . . Studies of phosphorus cycling in estuarine
sediments have mainly been based on measurements
of phosphate or total phosphorus concentrations
Ž Lebo and Sharp, 1992 . . However,
data on changes of various phosphorus fractions
Žcalcium bound to phosphorus and non-calcium
Table 1
Comparison of some physiographical characteristics of the
estuary over the two time periods considered
2
19871989 19931995
Area of drainage basin Ž km . 95 95
Longitudinal extent of estuary Ž km. 3.5 3.5
Tidal range Ž m. 1.0 1.0
1
Tidal frequency Ž day .
1.67 1.67
2
Estuarine surface Ž km .
4.5 3.75
Mean depth Ž m. 2.0 1.5
Tidal rangemean depth Ž m. 0.5 0.66
1
Rainfall Ž mm year .
8001050 25
3 1
River flow Ž m s .
8 4
Area covered by water Ž over 100% . 100 75
bound phosphorus and organic phosphorus. are
scarce in estuarine environments ŽRuttenberg,
1992; Ruttenberg and Berner, 1993 . .
In this study, the interannual pattern of variation
of the different fractions of phosphorus in
two periods Ž A. from 1987 to 1989 and Ž B. from
1993 to 1995 have been studied and will be related
to the water management strategies since
1987 and to the climatic changes described above,
to predict temporal trends in eutrophication. The
aim of this study is to describe the large scale
changes observed in the sediment of a small shallow
estuary Ž Palmones, Southern Spain. by measurements
of the different fractions of phosphorus.
2. Material and methods
2.1. Description of the study area
The Palmones River Estuary is located in
Southern Spain Ž Fig. 1. at the end of a small
catchment area. A comparison of some physiographic
characteristics of the estuary during the
two time periods considered is shown in Table 1.
Palmones is a well mixed shallow estuary Žmaxi-
mum depth 3.5 m. with a range of salinity from 29
to 35 Ž Clavero et al., 1997a . . The flow of freshwater
in the Palmones Estuary is dominated by
the Palmones River. At 23.5 km from the mouth
of the estuary is the dam mentioned above, which
started to store water in 1987. The results of
transformations cited above and the severe
drought in the last years, induced dramatic modifications
in the system Ž Tables 1 and 2 . .
2.2. Sampling and analytical methods
Sediment cores were taken monthly from March
1987 to November 1989 Ž Clavero, 1992. and quarterly
from March 1993 to March 1995, using three
PVC core tubes Ž 10 cm i.d., 15 cm long. inserted
by hand into the sediment, were retrieved and
covered in both extremes with silicone tops to
minimize the contact with the air and transported
to the laboratory in an icebox at 4C. In the
laboratory the sediment was extruded from the
cores and sliced in segments of 2 cm, under N2

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V. Claero et al. The Science of the Total Enironment 228 1999 193202 195
Table 2
Summary of average annual of some chemical and biological
variables analyzed over the two time periods considered.
P-flux were indicated as positive when released from the
sediment to the water and as negative when the P is
accumulated into the sediment
19871989 19931995
Water column
Phosphate Ž mol l . 2.50.7 8.152.1
Ammonium Ž mol l . 7.82.0 222
Nitrate Ž mol l
Sediment
.
9.81.3 175
Phosphate-flux 217491 27 to 220
Ž 2 1.
Calcium Ž mol l .
300700 25003000
Dissolved phosphate
1 Ž mol l .
165 15035
Organic matter Ž % .
30.8 142
Redox potential Ž mv. 180 220
Inorganic phosphorus
2 Ž IP, g m .
4.51 19070
Organic phosphorus
2 Ž OP, g m .
11.81.2 10749
Total phosphorus
2 Ž TP, g m .
Benthic organisms
16.32.3 297119
Zostera noltii Ž g dry wt. m . 100300 0
Ula rotundata Ž g dry wt. m . 0 50200
Hydrobia ulae Ž ind m . 10005000 700
Nereis diersicolor Ž ind m . 340900 0
1 a b
1 c b
1 c b
a b
mol m day 1 a c
a
See Clavero Ž 1992 . .
b
See Carreira et al. Ž 1995 . .
c
See Clavero et al. Ž 1997b . .
d
This study.
e
See Perez-Llorens ´
and Niell Ž 1990 . .
a b
a d
a b
a d
a d
a d
2 e b
2 b b
2 b b
2 a b
atmosphere. Each slice was dried at 60C for 24 h
and divided in two subsamples. One was used to
determine the inorganic phosphorus fractions
Ž Williams et al., 1971 . , non-calcium bound phosphorus
Ž NAIP. and calcium bound phosphorus
Ž AIP . . NAIP was the sum of CDB Žcitrate-
dithionite-bicarbonate. and NaOH extractable
phosphorus and AIP was extracted with HCl on
the residue after the previous treatment. So, the
total inorganic phosphorus Ž IP. was considered as
the sum of both fractions Ž NAIPAIP . .
The second subsample was used to determine
the organic phosphorus Ž OP. by extraction with
HClNaOH Ž Sommers et al., 1972 . . Soluble
phosphate was determined before and after the
digestion and the difference represented the con-
Ž .
centration of OP Sommers and Nelson, 1972 .
All the analysis of phosphate were made by means
of the malachite green method ŽFernandez
´ et al.,
1985. using a Technicon AAII.
2.3. Statistical analysis
Ž .
Two-way Analysis of Variance 0.05 were
used to compare the profiles in depth and time of
different fractions of phosphorus. Previously the
data were tested for normality using the G-test.
3. Results
Ž 2 The concentrations of AIP g m . over the
two periods of study are shown in Fig. 2. In the
period A values ranged between 1.25 and 2.50 g
m 2 . Maximum values were recorded in spring
1989 in the surface of the sediment. During period
B, the trend of AIP to increase in the sediment
is clear: 40 g m 2 in March 1993 rising to
100 g m 2 in March 1995. In Fig. 3 the time
series of NAIP concentrations are presented. The
values during the period A ranged between 2.0
and 3.0 g m 2 with maximum values at the end of
1987 and at the beginning of 1988. No values
obtained during the period A exceeded 3 g m 2 .
During B the concentration increased from 50 to
200 g m 2 . The depth profile of this fraction
showed a gradient with significant maximum values
at the surface.
The OP was three to four times more abundant
than the IP fraction in the sediment during A
Ž . 2
Fig. 4 and ranged between 10 and 14 g m .
Though the concentration of OP during B reached
50200 g m2 , an increase up to 15-times, OP
was less than the IP fraction Ž Fig. 5. during this
period.
The variations of the NAIP, AIP and OP with
time and depth were analyzed Ž two way ANOVA . ,
separately for each period. The results Ž Table 3.
showed that in both periods NAIP and OP concentrations
significantly increased with time and
depth, whereas only time trends of increase are
significant for AIP values indicating a homogeneous
depth distribution.
3.1. Integrated alues of NAIP, AIP and OP in
sediment.
The depth-integrated P concentrations was used

196
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V. Claero et al. The Science of the Total Enironment 228 1999 193202
Fig. 1. Map of Palmones River Estuary showing location of sampling station.
Ž . 2
Fig. 2. Seasonal changes in concentrations of calcium bound phosphorus AIP within the first 10 cm of sediment. Units are g m .

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V. Claero et al. The Science of the Total Enironment 228 1999 193202 197
Ž .
Fig. 3. Seasonal changes in concentrations of non-calcium bound phosphorus NAIP within the first 10 cm of sediment. Units are g
m 2 .
to calculate the percentage and the mass balance
of the different fractions. The percentages of
each fraction are shown over the whole time
study in Fig. 5. During A the most abundant
fraction was OP, which accounted for 6478% of
the total particulate phosphorus; NAIP ranged
between 12 and 20% and AIP from 8 to 15%. The
percentages during B are similar for NAIP and
OP, 3741%, whereas AIP accounted only for a
1924% of total. The ratio OP:IP Ž Fig. 6. ranged
between 2 and 3.5 during the period A and is
close to unity during B, expressing the progressive
increase of IP relative to CP. The addition of
depth-integrated P concentrations of NAIP, AIP
Ž . 2
Fig. 4. Seasonal changes in concentrations of organic phosphorus OP within the first 10 cm of sediment. Units are g m .

198
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V. Claero et al. The Science of the Total Enironment 228 1999 193202
Fig. 5. Seasonal changes in percentage of phosphorus fractions within the first 10 cm of sediment, using depth-integrated total
phosphorus concentrations.
and OP are shown in Fig. 7. During A, OP
concentrations were higher than IP. The OP values
ranged from 9 to 12 g m 2 , NAIP from 1.5 to
2.1 g m 2 and AIP from 1 to 1.5 g m 2 . After
1992 all fractions increased, mainly the NAIP and
AIP fractions which increased 75-fold. OP in-
creased 15 times this fraction and was more abun-
Ž .
dant in the recent observations March 1995 .
3.2. Mass balance calculations
Mass balance was obtained by making the integral
from surface to 10 cm in depth P-concentra-
tions, for each fraction and time interval. These
values obtained were plotted against time Ž year.
and the function that exhibited the best fit was
searched. The value of the first derivative Ž d Pdt.
of this function was considered to be the mass
Ž 2 1 balance g P m year . . Comparison of the
results obtained Ž Table 4. show an increasing
trend for all the fractions of phosphorus. During
the period A, accumulation was estimated at 0.52
gm 2 year 1 of OP; 0.40 g m 2 year 1 of NAIP;
and 0.26 g m 2 year 1 AIP, which means a total
phosphorus accumulation of 1.18 g m 2 year 1 .
During B, calculated values were 64.16 g m 2

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V. Claero et al. The Science of the Total Enironment 228 1999 193202 199
Table 3
ANOVA table from the data of different fractions of phosphorus
in the two time periods considered
Sv. 19871989 19931995
d.f. Fs d.f. Fs
NAIP
Time 08
a
21.31 06
a
22.7
Depth 05
a
2.52 05
a
3.17
Interaction
AIP
40
a
1.97 30
a
2.1
Time 08
a
49 06
a
31.73
Depth 05 1.1 ns 05 1.2 ns
Interaction
OP
40 0.89 ns 30 0.93 ns
Time 08
a
26.34 06
a
54
Depth 05
a
2.41 05 3 ns
Interaction
TP
40
a
2.2 30 1.03 ns
Time 08
a
11.58 06
a
73.8
Depth 05
a
2.69 05
a
6.5
Interaction 40
a
2.1 30
a
1.98
Note. Source of variation, Sv.; degrees of freedom, d.f.; Mean
a Ž .
squares ratio, Fs; significant, ; not significant ns for 0.05.
year 1 of NAIP; 31.6 g m 2 year 1 of AIP and
61.42 g m 2 year 1 of OP, and total phosphorus
accumulation was computed as 157 g m 2 year 1 .
4. Discussion
Organic phosphorus was the most abundant
fraction in the sediment at the end of the 1980s
and accounted for 70% of the total accumulated
phosphorus in the sediment of Palmones. These
results do not agree with the usual finding in
which the concentration of the inorganic fraction
is higher than the organic one ŽBostrom
¨ et al.,
1982 . . Accumulation of organic phosphorus can
occur by rapid phosphorus burial. The phosphorus
profiles Ž Clavero, 1992. found were related to
high productivity in the estuary, and to the consequently
increased organic matter settling on the
sediment. After 1992 organic matter in the sediment
increased fivefold and OP since this year
increased ninefold Ž Table 2 . . One possible explanation
of the increase of P concentration in the
sediment above the levels expected by organic
matter accumulation could be the lack of dilution
caused by P-poor inorganic particles that are retained
in the dam. The main sources of dissolved
phosphate in the interstitial water are the organic
fraction, through phosphatase activity ŽBerner,
1977; Froelich et al., 1979; Krom and Berner,
1981. and the bioavailabily inorganic phosphorus
Ž De Jonge et al., 1993 . . Phosphorus could also be
adsorbed onto solid particles ŽKrom
and Berner,
1981. and reprecipitate as calcium bound phosphorus
Ž AIP. or as labile phosphorus non-soluble
compounds NAIP Ž Jahnke et al., 1983. in water
with positive redox due to oxygen produced by
photosynthesis or aeration Ž Clavero et al., 1997c . .
Salinity favors adsorption onto particles in the
Ž .
Fig. 6. Seasonal changes in ratio of organicinorganic phosphorus OPAP using the depth integrated phosphorus concentrations
of different fractions.

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V. Claero et al. The Science of the Total Enironment 228 1999 193202
Fig. 7. Seasonal changes of mean Ž S.D. . of phosphorus fractions using the depth-integrated phosphorus concentrations. ŽNAIP,
.
2
non-Calcium Bound Phosphorus; AIP, Calcium Bound Phosphorus; OP, Organic Phosphorus . Units are g m . Insert is for the
early period.
Table 4
Mass balance calculations Ž 2 g P m 1 year . of different P
fractions over the two time periods considered
19871989 19931995
NAIP 0.40 58.3
AIP 0.26 31.6
OP 0.52 61.4
TP 1.18 157
sediment Ž Clavero et al., 1990, 1993. and Van
Cappellen and Berner Ž 1988. showed that the
limiting factor for calcium bound phosphorus production
would be an excess of phosphate related
to thermodynamic equilibrium. In Palmones estuary
the dissolved phosphate in the interstitial
water was in excess at equilibrium Ž Clavero, 1992 . .
A continuous accumulation of calcium bound
phosphorus exists in the sediment without significant
transformations, as the ANOVA indicated.
NAIP is the fraction that increased more
from period A to period B Ž Fig. 7 . . In this fraction
the labile forms of particulate phosphorus
are included and their solubilization is correlated
with reduced conditions. In Fig. 8 the NAIP fraction
presented a significant accumulation in the
sediment surface where it was easily mobilized
from sediment during period B and accumulated
at depth in period A.
The phosphate accumulated in sediment can be
released to the water column by resolubilization
of phosphorus under reduced conditions in the
sediment Ž Elderfield et al., 1981; Suess, 1981 . .
During the period A the phosphate was released
to the water column Ž Clavero et al., 1991, 1992.
but during the period B the direction of phosphate
exchange between sediment and water was
reversed. In both periods the sediment was under
reduced conditions Ž Table 2 . . This statement can
be explained by the influence of tidal cycle on the
phosphorus cycle in the estuary Ž Fig. 9 . . In the
period A, during flood tide a mean load of 1.79 g
s 1 enters in the estuary and the ebb has a mean
load of 1.95 g s 1 , This situation also is different
during the period B, in which the flood tide
enters a mean load of 3.6 g s 1 in the estuary,
whereas the ebb has a mean load of 0.13 g s1 Ž Carreira et al., 1995 . . The estuary is thus, located
between a bay which fertilizes it and a river
without water. The concentration of phosphate
increased because the reduced river flow did not
dilute it, while the tidal regime kept on fertilizing
it twice per day Ž Clavero et al., 1997a . . All the
changes noted in this study leads to modification
of benthic communities Ž Table 2 . : in 1989 Nereis
diersicolor accounted of all the animal biomass
in sediments Ž Clavero et al., 1991, 1992. and has
now disappeared; 10% of sediments was covered
by seagrass, Zostera noltii ŽPerez-Llorens
´
and
Niell, 1990. now up to 90% of sediment is cov-

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V. Claero et al. The Science of the Total Enironment 228 1999 193202 201
Ž . 2
Fig. 8. Seasonal changes of mean S.D. total phosphorus using depth-integrated phosphorus concentrations. Units are gm .
Insert is for the early period.
Fig. 9. Mean of phosphate exchange during a tidal cycle over the two time periods considered ŽData
of the period A, Guevara,
personal communication; the period B from Carreira et al., 1995 and modified from Clavero et al., 1997a . .
ered by Ula rotundata and the presence of seagrasses
is scarce; Hydrobia ulae densities have
sharply decreased and the red algae Gracilaria
rotundata which formed dense populations at the
bottom of the estuary has also disappeared. During
the period A, values of the freshwater input,
phosphate exchange, phosphorus into sediment
and mass balance in Palmones Estuary were similar
to other estuaries ŽFisher
et al., 1982; Boynton
et al., 1995 . . However, in the period B the values
of TP and MB were higher, up to 25- and 63-fold,
respectively to those quoted for other estuarine
systems. These values point out as Palmones is a
special system, being the typical example of the
estuaries of the subarid areas of southern Spain.
Acknowledgements
This work has been supported by the grant
AMB96-0782 of the Spanish Commission Interministery
Science and Technology.
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