Telechargé par Aicha Medjadba

African Journal of Aquatic Science Water

publicité
This article was downloaded by: [University of Milan], [Nadjla Chaib]
On: 21 June 2012, At: 13:21
Publisher: Taylor & Francis
Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer
House, 37-41 Mortimer Street, London W1T 3JH, UK
African Journal of Aquatic Science
Publication details, including instructions for authors and subscription information:
http://www.tandfonline.com/loi/taas20
Water quality assessment and application of the
biological diatom index in the Kebir-East wadi,
Algeria
a
b
N Chaïb & J Tison-Rosebery
a
Laboratoire de Recherche et de Conservation des Zones Humides (Université de
Guelma, Algeria), Faculté de Technologie, Université du 20 Août 1955, Skikda, Algeria
b
Cemagref Bordeaux, Unité de Recherche Réseaux, Epuration et Qualité des Eaux, 50
avenue de Verdun, 33610, Cestas, France
Available online: 02 Apr 2012
To cite this article: N Chaïb & J Tison-Rosebery (2012): Water quality assessment and application of the biological diatom
index in the Kebir-East wadi, Algeria, African Journal of Aquatic Science, 37:1, 59-69
To link to this article: http://dx.doi.org/10.2989/16085914.2011.636898
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching, and private study purposes. Any substantial or systematic
reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to
anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation that the contents
will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses
should be independently verified with primary sources. The publisher shall not be liable for any loss, actions,
claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or
indirectly in connection with or arising out of the use of this material.
African Journal of Aquatic Science 2012, 37(1): 59–69
Printed in South Africa — All rights reserved
Copyright © NISC (Pty) Ltd
AFRICAN JOURNAL OF
AQUATIC SCIENCE
ISSN 1608-5914 EISSN 1727-9364
http://dx.doi.org/10.2989/16085914.2011.636898
Water quality assessment and application of the biological diatom index in
the Kebir-East wadi, Algeria
N Chaïb1* and J Tison-Rosebery2
Faculté de Technologie, Université du 20 Août 1955 Skikda, Algeria. Laboratoire de Recherche et de Conservation des Zones
Humides, Université de Guelma.
2 Cemagref Bordeaux, Unité de Recherche Réseaux, Epuration et Qualité des Eaux, 50 avenue de Verdun, 33610 Cestas, France
* Corresponding author, e-mail: [email protected]
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
1
A total of 118 benthic diatom taxa were recorded during a survey in 2007 of the Kebir-East wadi, north-eastern
Algeria. Fourteen samples were collected at seven sampling stations in winter and summer. The majority of diatom
taxa comprised cosmopolitan species widely distributed along the hydrosystem. Canonical correspondence analysis,
used to examine spatial patterns of diatom communities in relation to environmental gradients, was statistically
highly significant (p < 0.001). The first axis accounted for 45% and the second for 22% of the total variance. Seasonal
and physicochemical gradients were clearly defined and indicated the water quality. A cluster analysis was then
carried out to represent the different groups of the sampled stations sharing the same flora. Agglomerative cluster
analysis grouped the sampled sites into seven clusters according to the community data. For clusters gathering
more than one single sample, typical diatom taxa were determined with an indicator species analysis. The reliability
of the biological diatom index BDI 2007 was tested under our environmental conditions and it was concluded that,
considering the very particular geochemical context of this wadi, a specific diatom index should be developed.
Keywords: BDI 2007, canonical correspondence analysis, cluster analysis, environmental gradients, IndVal analysis
Introduction
The biotic components of running water systems are
important parameters for the assessment of water quality
(Stanford and Ward 1988, Junk 1999, Stoermer and Smol
1999, de la Rey et al. 2008). To assess the ecological status
of water bodies, taxonomic composition, abundance and the
ratio of sensitive to insensitive taxa have to be considered
as biological indicators of water quality. However, knowledge
of the biotic components of North African rivers or wadis is
relatively poor and these water systems remain some of the
least-studied Mediterranean ecosystems. Up to now Algerian
wadis have been scantily studied, particularly concerning
their ecological aspects (e.g. Lounaci et al. 2000), even
if they represent interesting natural conditions as they
are strongly influenced by an accentuated Mediterranean
climate, including extreme temperature values during
summer and short, extreme flooding events followed by long
dry periods. There is a considerable lack of knowledge about
possible environmental conditions and biological changes
that these hydrosystems are likely to experience in the light
of pollution or climatic changes. Most studies of Algerian
wadis have been confined to their physicochemical characteristics and macroinvertebrates (Lounaci et al. 2000, Belaidi
et al. 2004), whereas studies on algae, particularly diatoms,
are rare (Baudrimont 1973).
Diatoms are a key component of aquatic ecosystems.
They respond directly and rapidly to many environmental
parameters such as geology (Stevenson 1997, Pan et al.
2000), current velocity (Peterson and Stevenson 1990),
and nutrients (Potapova and Charles 2003). Their speciesspecific sensitivity to different parameters varies according to
species physiology, leading to a large group of assemblage
compositions according to ecological conditions (Licursi
and Gomez 2002, Potapova and Charles 2002, Tison et al.
2005). Knowledge of how the interactions of geographical
and environmental factors drive the distribution patterns of
benthic diatom species in Algerian wadis is crucial for the
development of future water quality assessment tools that
are adapted to this particular context.
The aims of the present study were to survey the benthic
diatom communities of the Kebir-East wadi, to relate their
distributional patterns to environmental variables, and to test
the reliability of the biological diatom index in this instance
(Lenoir and Coste 1996, Coste et al. 2009).
Materials and methods
Study area
The Kebir-East wadi, north-eastern Algeria, extends over a
length of 96 km from the junction of Leben and Mellili wadis
in the east to its confluence with the Mafragh River in the
west (Figure 1). The climate is typically Mediterranean with
a dry and hot summer and with rainfall occurring mostly
during the winter months.
The Kebir-East wadi represents a mosaic of geomorphodynamic natural conditions, as well as diverse levels
of man-made disturbances of a variety of origins (physical:
African Journal of Aquatic Science is co-published by NISC (Pty) Ltd and Taylor & Francis
Chaïb and Tison-Rosebery
60
7° E
8°15′ E
8°30′ E
MEDITERRANEAN SEA
Boumershene
10 km
Messida
Aïn Assel
B
D
Gu
erg
ou
r
Da
rda
n
Bou
Lath
an
M
af
ra
gh
5
C
ir-E
a
E
Bouteldja
36°50′ N
Ke
ad
st W
b
El Tarf
i
A
Le
be
n
Mellili
36°45′ N
MEDITERRANEAN SEA
Mexa
Dam
Enlarged area
s
ou
ug
Bo
ed
Qu
ALGERIA
Zito
un
LEGEND
Sampling site
Wadi
River
r
ua
Lo
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
F
Wa
EL TARF
0
Lake
Oubeira
G
di
Bo
urd
im
Kebir-E
ast
TUNISIA
De
gr
ah
ALGERIA
Algeria
AFRICA
Figure 1: Map of the study area indicating locations of sites in the Kebir-East wadi, north-eastern Algeria, sampled in 2007
Bouhalloufa and Mexa dams; chemical: presence of
non-point pollutions, and municipal wastes). The substratum
of the Kebir-East wadi is composed either of ancient
sediments (marls and sandstone) of the Algerian local
marine Miocene (equivalent to the continental Aquitanien),
degraded slightly on the surface in the east, or more recent
Plio–Quaternary sediments corresponding to alluviums of
the high and average terraces of the Kebir-East wadi valley.
The recent Quaternary sediments in the valley of Kebir-East
wadi comprise silt, sand and stones (Marre 1987).
Over the winter and summer of 2007, a total of 14 samples
were examined (see Table 1). Seven sampling sites were
selected across a gradient of pollution from near farmlands
and from near-pristine to heavily urbanised areas. The sites
sampled on the main course of the Kebir-East wadi (Figure 1)
show a wide range of conductivity (300–900 μS cm−1),
alkalinity (16–128 mg l−1 of CaCO3), and pH (6.5–8.3). The
particular geochemical context leads to high conductivities
(>500 μS cm−1) often associated with low pH (<7).
Farmlands surround the Kebir-East wadi, and the
farmers use a considerable amount of water to irrigate
their farms and provide drinking water for their cattle.
Sampling sites are characterised by deep and fast-flowing
waters during the winter and shallow slow-flowing waters
during the summer. Station A was situated within the
El Kala National Park (PNEK), created in 1983, added to
the National Heritage list and classified as a Biosphere
Reserve by UNESCO in 1990. The Kebir-East wadi in this
non-urbanised area is surrounded by farmlands and flows
on a sandstone land. Station B at Aïn Assel, situated not far
from Mexa dam, is transformed into pools in summer and
autumn. The presence of slaughterhouses near Stations
C and E impacts the water quality of the Kebir-East wadi,
in addition to municipal wastes of Aïn Khiar and Bouteldja
towns, which discharge directly into the wadi. Station D
receives the polluted water of Guergour wadi, which is
highly impacted by sewage of the Guergour conglomeration.
Stations F and G, located at Righia and Sebaa conglomerations, respectively, were also surrounded by farmlands.
The waters of these stations were deeper (0.5–1.6 m), and
the flow velocities recorded were high in winter and low in
summer.
Dataset
Samples of diatoms were collected according to a standardised method, NFT90-354 (AFNOR 2000), from five randomly
chosen stones representing a total surface area of 100 cm2.
The stones were scraped with a toothbrush and the pooled
material was stored in dark bottles containing 5% formaldehyde. Diatom species were identified at 1 000× magnification under a Zeiss light microscope (400 valves per slide),
by examining permanent slides of cleaned diatom frustules,
digested in boiling H2O2 (30%), and HCl (35%), and mounted
in a high refractive index medium (Nafrax, RI = 1.74).
Taxa were identified according to Süsswasserflora von
Mitteleuropa (Krammer and Lange-Bertalot 1985–1991)
and complementary works (Patrick and Reimer 1966, 1975,
Germain 1981, Hartley et al. 1996, Kelly 2000).
Water quality measurements and water samples were
collected during the winter and summer seasons of 2007
at each site. Sixteen water quality variables (pH, conductivity, turbidity, oxygen saturation, dissolved oxygen, current
velocity, temperature, alkalinity, nitrates, nitrites, orthophosphates, sulphates, chlorides, ammonium, calcium and
116.0
116.5
142.5
120.0
26.0
20.0
76.0
145.0
22.0
17.0
27.0
35.0
119.5
123.0
114.0
77.0
86.0
138.0
72.0
51.0
118.0
59.0
77.0
29.0
134.0
47.0
83.0
33.0
217.0
185.0
159.5
190.0
133.0
16.5
131.0
167.0
128.0
125.0
178.0
116.0
155.0
120.0
6.8
7.2
7.3
6.5
6.9
6.7
8.3
7.1
7.1
6.8
7.4
7.0
6.6
6.9
SO4
Ca
Mg
(mg l−1) (mg l−1) (mg l−1)
pH
A
B
C
D
E
F
G
KebAs
KebAK
KebGrg
KebAn
KebRg
KebSb
Kebir at
R’Mel Souk
Kebir at
Ain Assel
Kebir at
Ain Khiar
Kebir at
Guergour
Kebir at
Ouled Anenes
Kebir at
Righia
Kebir at
Sebaa
KeRSk
S
W
S
W
S
W
S
W
S
W
S
W
S
W
12.0
9.2
16.4
17.2
21.7
21.0
19.8
5.5
7.9
7.8
10.3
10.3
7.9
8.2
0.3
0.2
0.8
0.4
0.1
0.3
0.2
0.2
1.2
0.6
1.4
0.8
0.6
0.4
0.2
0.1
1.0
0.1
0.6
0.6
0.0
0.7
0.2
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.5
1.2
0.7
0.4
3.1
0.6
0.9
0.9
1.1
0.9
1.1
1.0
42.0
97.0
1 065.5
217.0
534.0
87.0
288.0
257.0
970.0
124.0
97.0
654.0
336.0
176.0
19.4
63.8
4.0
38.8
13.0
31.9
11.5
44.3
10.3
37.1
14.6
39.1
11.4
25.0
155.4
160.7
109.6
145.8
91.4
101.1
113.3
136.7
111.0
102.4
111.5
102.5
110.1
109.3
15.6
18.7
11.6
16.8
8.2
11.6
10.5
16.2
10.1
11.6
9.8
11.7
10.6
12.5
15.0
8.6
17.6
9.0
20.6
9.2
18.7
7.9
19.9
9.7
21.6
9.4
17.0
9.3
225.0
162.0
93.0
158.0
103.0
114.2
159.0
247.0
105.0
210.0
111.0
171.0
144.0
118.0
768.0
771.0
556.5
380.0
680.0
416.0
864.0
683.0
759.0
1 048.0
760.0
407.0
758.0
386.0
TAC
(mg l−1
CaCO3)
68.0
58.0
96.5
128.0
50.0
27.0
48.0
92.0
31.0
20.0
20.0
40.0
43.0
17.0
Temp
Cl
Cond
(°C) (mg l−1) (μS cm−1)
O2dis
(mg l−1)
O2sat
(%)
Currvel
(cm s−1)
Turb
(NTU)
NO2
NH4
PO4
(mg l−1) (mg l−1) (mg l−1)
NO3
(mg l−1)
Stn Season
Site
code
Data analysis
Relative abundances of species were transformed by
natural algorithm in order to reduce their variation range. To
avoid a problem of logarithm zeroes, the value 1 was added
to each abundance.
Groups of samples sharing the same type of community
composition were defined using a hierarchical cluster
analysis (Goodall 1973), with Ward’s linkage method and
Euclidian distance measure. Multi-response permutation procedures (MRPP; Biondini et al. 1985) were used to
test the reliability of the groups obtained. Typical species
for each cluster were determined with an indicator species
analysis (IndVal; Dufrêne and Legendre 1997). This method
combines information on the concentration of species
abundances in a particular group and the faithfulness of
occurrence of a species in a particular group. Indicator
values were tested for statistical significance using a
randomisation (Monte Carlo) technique (McCune and Grace
2002). Agglomerative cluster analysis, MRPP and indicator
species analysis were performed with the software PCord
4.25 (McCune and Mefford 1999).
To look for ecological determinants of diatom
assemblages along the Kebir-East, we used canonical
correspondence analyses (CCA; ter Braak 1986, ter Braak
and Verdonschot 1995), a two-table ordination method
performed using the ADE-4 package in the R environment (Thioulouse et al. 1997, Thioulouse and Dray 2007,
R Development Core Team 2009). This multivariate analysis
tool has been used to ordinate samples by searching for a
co-structure between physicochemical variables and diatom
species. The correlation in CCA was carried out between
the two new sets of projected coordinates. The significance of the resulting correlation (R-value) between the two
sets of coordinates resulting from the CCA was tested by
carrying out 1 000 canonical correspondence analyses of
the environmental descriptors and the diatom datasets after
random permutations of their rows (ter Braak 1986).
Cluster and indicator species analysis results were used
for the interpretation of the CCA graph and to highlight the
more typical species. Cluster memberships were specified
on the CCA graph and indicator species were underlined.
The biological diatom index (BDI 2007) scores were
determined using OMNIDIA 5.3 (http://omnidia.free.fr). For
each sample, the community of diatoms was described with
species relative abundance.
Richness, diversity and evenness indices were also
calculated (Shannon and Weaver 1949). Evenness
accounts for both abundance and evenness of the species
present, and assumes a value between 0 and 1 with 1 being
complete evenness.
Site
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
magnesium) were measured at mid-depth where the diatoms
were collected. All chemical variables were analysed with
a laboratory photometer 5000 according to the colorimetric
method, and measured in mg l−1. Temperature and conductivity were measured in situ with an Ecoscan con5 conductimeter. Water pH was measured using a 209-HANNA pH
meter. Turbidity was measured with an Aqualytic turbidimeter. Saturation and dissolved oxygen were measured with
an oxymeter. The current velocity was measured vertically
with a Global Flow Probe (FP101-FP201).
61
Table 1: Physicochemical variables of water at the Kebir-East wadi sampling sites in winter and summer 2007. Stn = station (see Figure 1), S = summer, W = winter, Turb = turbidity,
Currvel = current velocity, O2sat = saturation of oxygen, O2dis = dissolved oxygen, Cond = conductivity, TAC = alkalinity
African Journal of Aquatic Science 2012, 37(1): 59–69
Chaïb and Tison-Rosebery
62
Results
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
The 118 diatom taxa from 43 genera determined from our
14 samples belong to the key taxa list used by BDI 2007.
See Appendices 1 and 2 for diatom species abbreviations
and counts, and Table 2 for floristic diversity and BDI 2007
values. Ecological characteristics of species were derived
from van Dam et al. (1994). Measured values for the
physical and chemical variables (n = 14) in the Kebir-East
wadi are presented in Table 1.
The agglomerative cluster analysis (Figure 2) grouped
the sampled sites into clusters according to the community
data. We chose the seven-groups level of the dendrogram,
Table 2: Floristic diversity and BDI 2007 values for the sampling
sites in summer and winter 2007. See Table 1 for site codes (S =
summer, W winter)
Site code
KeRSkS
KebAKS
KeRSkW
KebSbW
KebAKW
KebGrgW
KebRgW
KebGrgS
KebSbS
KebAsW
KebRgS
KebAnS
KebAnW
KebAsS
Total
Richness Diversity Evenness
counted
409
46
4.26
0.77
402
45
4.22
0.77
401
50
4.31
0.76
402
50
4.38
0.78
400
47
4.11
0.74
406
41
4.07
0.76
400
43
3.93
0.72
401
55
4.46
0.77
408
42
4.13
0.77
400
50
4.16
0.74
400
43
4.39
0.81
426
27
2.87
0.60
408
29
3.11
0.64
414
16
1.47
0.37
BDI
2007
11.7
11.8
11.0
11.6
11.3
10.7
9.9
11.6
10.9
11.9
9.2
8.0
8.0
18.0
the MRPP results showing that the groups obtained were
statistically different (A = 0.303, p < 0.005). For clusters
gathering more than one single sample, typical species were
determined with an indicator species analysis. Indicator
values are given in Table 3, along with statistical significance values calculated by randomisation (Monte Carlo)
Table 3: Diatom indicator species by group (IndVal analysis). See
Appendix 1 for explanation of species codes
Species
Group
Value
CEUG
1
100.0
CPLA
1
100.0
NPAL
1
39.3
NCTV
1
49.2
NGRE
1
50.4
NDIS
1
51.0
NLAN
1
51.5
SBRE
1
52.0
CPED
1
54.5
TAPI
1
56.2
CSOL
1
66.4
NCTO
1
71.7
MALC
3
100.0
NCPL
3
100.0
GPUM
3
50.9
CMEN
3
70.0
NCPR
3
76.8
CTUM
6
100.0
NIFR
6
38.0
NRCS
6
62.2
NFIC
6
73.8
PSBR
6
76.1
SEMN
6
79.2
* Significance levels of the permutation tests
p*
0.0390
0.0390
0.0410
0.0420
0.0490
0.0280
0.0550
0.0210
0.0430
0.0180
0.0340
0.0200
0.0050
0.0050
0.0180
0.0250
0.0160
0.0430
0.0160
0.0520
0.0120
0.0100
0.0290
DISTANCE (objective function)
2.8E+00
3.6E+01
100
75
7E+01
1E+02
1.4E+02
25
0
INFORMATION REMAINING (%)
50
KeRSkS
KebAKS
KebGrgS
KeRSkW
KebAsW
KebAKW
KebGrgW
KebRgW
KebSbW
KebAsS
KebRgS
KebAnS
KebAnW
KebSbS
Figure 2: Agglomerative cluster dendrogram based on diatom communities sampled in the Kebir-East wadi in 2007. IndVal was calculated for
the three clusters (1, 3 and 6) that gathered more than one sample. See Table 1 for site codes (S= summer, W = winter) and Table 3 for results
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
African Journal of Aquatic Science 2012, 37(1): 59–69
(McCune and Grace 2002). Indicator species are shown on
the CCA graph (underlined codes).
Taxa were mostly alcaliphilic, eutraphentic (respectively 69.9 ± 18.1% and 52.5 ± 16% of the average sample
composition), and cosmopolitan, showing no particular
endemism. Samples with low pH (<7) and high conductivity
(>500 μs cm−1) were frequent, where acidophilus species
were very rare (e.g. the sample KebSbS where pH = 6.7
showed the higher proportion of acidophilus species with
only one Eunotia arcus [EARC], two Eunotia implicata
[EIMP] and one Encyonema neogracile [ENNG]), whereas
alcaliphilic and halophilous species were dominant.
Richness ranged from 16 to 55, and diversity from 1.47 to
4.46. Evenness values were high except for sample KebAsS
(see Table 2).
The CCA, carried out with 16 environmental variables
and 118 diatom species, highlighted the links between the
environmental characteristics of the Kebir-East wadi and
the different diatom species, and clearly ordered the 14
sites. Figure 3 shows the 70 principal species across the
14 sampled sites (species that were present at a minimum
of three sites). As shown by Monte Carlo simulations, the
CCA was statistically highly significant (p < 0.001). The first
axis accounted for 45%, and the second for 22%, of the
total variance.
Axis 1 separated the well-oxygenated sites with high
alkalinity and current velocity that were characterised by the
presence of Rhoicosphenia abbreviata (RABB), Amphora
pediculus (APED), Diatoma vulgaris (DVUL), and Navicula
lanceolata (NLAN), from the sites with lower current velocity,
strong water conductivity and high chlorides concentration.
These sites were also rich in nutrients and related to anthropogenic stress, with species such as Nitzschia frustulum
(NIFR), Ulnaria ulna (UULN), Nitzschia filiformis var.
conferta (NFIC), Sellaphora minima (SEMN), and Navicula
recens (NRCS).
A seasonal gradient was apparent along the second axis.
The sites sampled in winter were plotted on the positive part
of the axis, and were characterised by the abundance of
species such as Mayamaea alcimonica (MALC), Navicula
capitatoradiata (NCPR), Gomphonema pumilum (GPUM),
and Cyclotella meneghiniana (CMEN). The sites sampled
in summer were plotted in the negative part of the axis
and were dominated by the presence of species such as
Cocconeis euglypta (CEUG), Cocconeis placentula (CPLA),
Cymatopleura solea (CSOL), Nitzschia dissipata (NDIS),
and Cyclotella ocellata (COCE).
Globally, winter samples reflected the higher current
velocities and dissolved oxygen rates, as well as the higher
proportion of halophilous species (57.1 ± 5.4%).
Station E did not show this seasonal variation, where
samples from winter and summer both had low current
velocity and shared more or less the same diatom community.
Low richness and diversity, and the lowest BDI 2007 scores
were recorded at this station.
Sample KebAsS was particularly notable as the abundance
of Achanthidium minutissimum (ADMI) reached 75% of the
total effective (low evenness values). As a consequence the
corresponding BDI 2007 score was very high (18/20) but did
not reflect the water quality of this station. This station was
transformed into temporary pools during the dry seasons.
63
Discussion
Assessing the ecological integrity of running waters often
requires the development of integrated methods that
consider the complex interrelationships between both
community assemblages and the variability of environmental
factors. The relations between diatoms and environmental
variables are robust and quantifiable, making diatoms
appropriate quantitative indicators of ecological conditions
in lotic systems (Pan et al. 1996, Oliveira et al. 2001).
In the present study, associations between diatom
assemblages and environmental variables of the Kebir-East
wadi, a North African hydrosystem, were detected through
CCA, cluster and indicator species analyses. Seasonal
and physicochemical gradients were clearly defined and
reflected the water quality.
Our floristic results are in agreement with those of
Baudrimont (1973), who enumerated 206 diatom taxa from
65 sampling stations of freshwater and brackish waters from
Algeria (seven stations in the chotts, 34 in the Sahara [arid
and semi-arid climates], 14 stations from thermal mineral
waters [up to 80 °C] and 10 stations from northern Algeria
[reservoirs and wadis]). Baudrimont (1973) studied the
spatial distribution of the diatom species and their relation to
the physicochemical water quality of the sampled stations,
but not their seasonal variations. Most of the species cited
by Baudrimont (1973) are cosmopolitan and typical of
high-conductivity and eutrophic waters. His results highlight
that the Algerian diatom flora is comparable to the European
flora, but he noticed a particular adaptation of the species
resulting in a better tolerance to high salinity and alkalinity.
Lange-Bertalot (2009) found and described four new
species of the recently established genus Navigiolum from
samples collected in ephemeral rock pools in Algeria.
Similar to Baudrimont, we did not find such species in our
samples perhaps because, to date and in this country,
Navigiolum taxa have been found only in oligosaprobic and
oligohalobious waters.
The diatom communities from the Kebir-East wadi were
particularly interesting in that they responded to unusual
environmental conditions: a high seasonal gradient between
floods and drought, and acidic to neutral waters together
with high conductivities. As a consequence, in the present
study we observed first a clear separation between winter
and summer communities, except for Station E at Ouled
Anenes where water chemistry and flow did not significantly
change from winter to summer (low current velocity and
high conductivity).
This clear temporal axis on the CCA discriminates rheophilic
species occurring with high discharges mainly in winter,
and standing water species preferring low discharge and
high chloride concentrations in summer. The same conclusions are reported in Aboal et al. (1996) with respect to some
Mediterranean temporary streams in south-eastern Spain.
The most radical difference between winter and summer
communities appears at Station B at Ain Assel, where the
Kebir-East wadi is transformed into isolated pools in summer,
with high turbidity levels. Achnanthidium minutissimum (ADMI)
during this season represents up to 75% of the community
abundance. This species has already been reported as
typical of intermittent rivers transformed into a series of
Chaïb and Tison-Rosebery
64
(a)
KebSbW (3)
KebRgW (3)
KebAKW (3)
KebGrgW (3)
KebAnW (6)
KebAsW (3)
KebSbS (6)
KeRSkW (3)
KebAnS
KebAKS (1)
KebRgS
KebAsS
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
KebGrgS
KeRSkS (1)
(b)
MALC
DMON
MPMI
Turbidity
NIFR
NCPR
GPUM
RABB
NCTE
GPAR
NACI
DELL
ENNG
ADEU
NCPL
NILA
NDES
NSUA
CPLI
PO4
LGOE
CTUM
UULN
NGER
NFIC
SEMN
ESLE
NRCS PSBR ADEG
NH4
NSHR
NVDS
BPAX
pH
RSIN
NGES
NCRY
ESUM
Currvel
NLAN
TAPI
PLEV
CSOL
GEXL
CPED
O2%sat
ADLA
NDIS
HVEN
NO2
O2dis
SBRE
NAAM
GMIN
ESBM
DVUL
Alkalinity
Ca
NVDA
Cl
NGRE
APED
FPYG
NVEN
Conductivity
SO4
NPAL
DPST
NCTV
ADSA
Mg
AUGR
NAMP
GOLI
CMEN
ADMI
COCE
NCTO
NROS
Temperature
NO3
FCVA
CEUG
CPLA
NTPT
Figure 3: Canonical correspondence analysis of 14 samples from the Kebir-East wadi in 2007, including 70 diatom taxa (present at a
minimum of three stations) and 16 physicochemical variables. (a) Site scores (based on water quality): the solid ellipse groups winter samples
and the dashed ellipse groups summer samples; cluster memberships are given in brackets; see Table 1 for site codes (S = summer, W =
winter); (b) species scores (indicator species underlined) and environmental gradients; see Appendix 1 for species abbreviations
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
African Journal of Aquatic Science 2012, 37(1): 59–69
ponds in summer (Aboal et al. 1996, Garcia et al. 2008, Boix
et al. 2010). Achnanthidium minutissimum, well known as a
cosmopolitan pioneer (early coloniser) in disturbed environments (Passy and Bode 2004), can be considered resistant to
high and frequent changes in current velocities.
The second pecularity of the Kebir-East wadi environmental conditions is the high average value of conductivity levels, even in undisturbed conditions, together with
near-neutral to acidic pH values. This leads to the quasiabsence of the genera Eunotia and Brachysira, known to
be acidophilus (van Dam et al. 1994), whereas alkaliphilic
species tolerant to quite high conductivity are dominant
(Surirella brebissonii [SBRE], Nitzschia frustulum [NIFR]
for example), and even halophilous species such as
Tryblionella apiculata (TAPI).
As a consequence, the reliability of the BDI 2007 (Lenoir
and Coste 1996, Coste et al. 2009) to assess the water
quality of the Kebir-East wadi is disputable. BDI 2007 was
developed in France, and its notation system is based on
species ecological profiles established from a dataset of
typical French environmental conditions. In the present
dataset, samples with such high conductivities and low pH
in natural conditions are absent, and then tolerant species
towards high conductivities are systematically associated
with an anthropogenic impact.
This may be an explanation of the quite low BDI 2007
scores (11.7/20 in summer and 11/20 in winter) obtained for
the Station at Kébir at R’Mel Souk, yet situated within the El
Kala National Park and showing very low levels of anthropogenic influence (Table 1).
BDI 2007 scores in this study were not contrasted
enough, and do not appear to be in correspondence with
the water quality gradient, where high conductivities and
associated species tended to confuse the biological integrity
signal. The highest score (18/20) was obtained at Ain Assel
in summer, where Achanthidium minutissimum (ADMI) was
dominant, and did not reflect the real poor water quality of
that station ([NH4+] = 1 mg l−1, [PO43− ] = 0.5 mg l−1). In BDI
2007 Achanthidium minutissimum is considered as typical
of quite good water qualities and, as intermittent streams
are very scarce in France, has never been associated with
drought events. Ecological characteristics of diatoms seem
not to be universal, and rather are only valid for specific
regions (Potapova and Charles 2007).
Conclusion
The particular environmental context of the Kebir-East wadi
led to unusual diatom assemblages, driven by high seasonal
gradients between floods and droughts, and acidic to neutral
waters together with high conductivities even at undisturbed
sites. As a consequence, in this study BDI 2007 scores do
not appear to be in correspondence with the water quality
gradients, even if the 118 identified species are cosmopolitan
and all belong to the BDI 2007 key species list. This Algerian
hydrosystem needs to be studied thoroughly, and largerscale surveys must be carried out over winter and summer
seasons in order to achieve a natural typology of the rivers
and to build typical species ecological profiles. A specific
diatom-based index could subsequently be developed,
eventually following the approach used to build the BDI 2007.
65
Acknowledgements — This research was funded in part by the
Algerian Ministère de l’Enseignement Supérieur et de la Recherche
Scientifique (MESRS) and by the Unité de Recherche Réseaux,
Epuration et Qualité des Eaux, CEMAGREF Bordeaux (France).
We thank the manager and engineers of the National Park of El
Kala (Algeria), who allowed us to access the protected areas for
sample collection, and for their advice and documentation. We
thank Michel Coste for his kind help concerning diatom taxonomy.
We are also grateful for the improvements that the referees brought
to previous versions of the manuscript.
References
Aboal M, Puig MA, Soler G. 1996. Diatom assemblages in some
Mediterranean temporary streams in southeastern Spain. Archiv
für Hydrobiologie 136: 509–527.
AFNOR (Association Française de Normalisation). 2000. Norme
Française NFT 90-354. Détermination de l’Indice Biologique
Diatomées (IBD). Paris: AFNOR.
Baudrimont R. 1973. Précisions sur l’écologie en Algérie, de
Terpsinoe musica Her. (Bacillariophycées Anaulacées). Bulletin
de la Société Linnéenne 3: 21–24.
Belaidi N, Taleb A, Gagneur J. 2004. Composition and dynamics of
hyporheic and surface fauna in a semi-arid stream in relation to
the management of a polluted reservoir. International Journal of
Limnology 40: 237–248.
Biondini ME, Bonham CD, Redente EF. 1985. Secondary successional patterns in a sagebrush (Artemisia tridentata) community
as they relate to soil disturbance and soil biological activity.
Vegetation 60: 25–36.
Boix D, Garcia-Berthou E, Gascon S, Benejam L, Tornès E, Sala
J, Benito J, Munné A, Solà C, Sabater S. 2010. Response of
community structure to sustained drought in Mediterranean rivers.
Journal of Hydrology 383: 135–146.
Coste M, Boutry S, Tison-Rosebery J, Delmas F. 2009. Improvements of the Biological Diatom Index (BDI): description and
efficiency of the new version (BDI-2006). Ecological Indicators 9:
621–650.
de la Rey PA, Roux H, van Rensburg L, Vosloo A. 2008. On the
use of diatom-based biological monitoring. Part 2: A comparison
of the response of SASS 5 and diatom indices to water quality
and habitat variation. Water SA 34: 61–69.
Dufrêne M, Legendre P. 1997. Species assemblages and indicator
species: the need for a flexible asymmetrical approach. Ecological
Monographs 67: 345–366.
Garcia L, Delgado C, Pardo I. 2008. Seasonal changes of benthic
communities in a temporary stream of Ibiza (Balearic Islands).
Limnetica 27: 259–272.
Germain H. 1981. Flore des Diatomées. Diatomophycées eaux
douces et saumâtres du Massif Armoricain et des contrées
voisines d’Europe occidentale. Paris: Boubée.
Goodall DW. 1973. Numerical classification. In: Whittaker RH
(ed), Handbook of vegetation science, part 5: Ordination and
classification of communities. The Hague: Dr W Junk. pp 575–615.
Hartley B, Barber HG, Carter JR, Sims PA. 1996. An atlas of British
diatoms. Bristol: Biopress.
Junk WJ. 1999. The flood pulse concept of large rivers: learning
from the tropics. Archiv für Hydrobiologie 115: 261–280.
Kelly MG. 2000. Identification of common benthic diatoms in rivers.
Field Studies Council 9: 583–700.
Krammer K, Lange-Bertalot H. 1985–1991. Bacillariophyceae.
Süsswasserflora von Mitteleuropa, Band 2 (part 1–4). Stuttgart:
Gustav Fisher Verlag.
Lange-Bertalot H, Fumanti B, Cavacini P, Tagliaventi N. 2009. The
genus Navigiolum (Bacillariophyceae) in Mediterranean and
North African rock pool habitats: description of four new species
from Algeria. Fottea 9: 179–185.
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
66
Lenoir A, Coste M. 1996. Development of a practical diatom index
of overall water quality applicable to the French National Water
Board Network. In: Whitton BA, Rott E (eds), Use of algae for
monitoring rivers II. Innsbruck: Institut für Botanik, Universität
Innsbruck. pp 29–43.
Licursi M, Gomez N. 2002. Benthic diatoms and some
environmental conditions in three lowland streams. International
Journal of Limnology 38: 109–118.
Lounaci A, Brosse S, Mouloud SA, Lounaci-Daoudi D, Mebarki
N, Thomas A. 2000. Current knowledge of benthic macroinvertebrate diversity in Algerian streams, a species check list of the
Sébaou River basin (Tizi Ouzou). Bulletin de la Société d’Histoire
Naturelle (Toulouse) 136: 43–55.
Marre A. 1987. Le Tell oriental algérien de Collo à la frontière
tunisienne: étude géomorphologique. PhD thesis, Université d’Aixen-Provence, France.
McCune B, Grace JB. 2002. Analysis of ecological communities.
Gleneden Beach, Oregon: MjM Software.
McCune B, Mefford MJ. 1999. Multivariate analysis of ecological
data, version 4.01. Gleneden Beach, Oregon: MjM Software.
Oliveira MA, Torgan LC, Lobo EA, Scharzbold A. 2001. Association of
periphytic diatom species of artificial substrate in lotic environments
in the Arroio Sampaio Basin, RS, Brazil: relationships with abiotic
variables. Brazilian Journal of Biology 61: 523–540.
Pan Y, Stevenson RJ, Hill BH, Herlihy AT, Collins GB. 1996. Using
diatoms as indicators of ecological conditions in lotic systems: a
regional assessment. Journal of the North American Benthological
Society 15: 481–495.
Pan Y, Stevenson RJ, Vaithiyanathan P, Slate J, Richardson
CJ. 2000. Changes in algal assemblages along observed and
experimental phosphorus gradients in a subtropical wetland,
USA. Freshwater Biology 44:339–354.
Passy SI, Bode RW. 2004. Diatom Model Affinity (DMA), a new
index for water quality assessment. Hydrobiologia 524: 241–251.
Patrick R, Reimer CW. 1966. The diatoms of the United States,
exclusive of Alaska and Hawaii, vol. 1. Monographs of the
Academy of Natural Sciences of Philadelphia 13: 1–699.
Patrick R, Reimer CW. 1975. The diatoms of the United States,
exclusive of Alaska and Hawaii, vol. 2, part 1. Monographs of the
Academy of Natural Sciences of Philadelphia 13: 1–21.
Peterson CG, Stevenson RJ. 1990. Post-spate development of
epilithic algal communities in different current environments.
Chaïb and Tison-Rosebery
Canadian Journal of Botany 68: 2092–2102.
Potapova M, Charles DF. 2002. Benthic diatoms in USA rivers:
distributions along spatial and environmental gradients. Journal
of Biogeography 29: 167–187.
Potapova M, Charles DF. 2003. Distribution of benthic diatoms
in US rivers in relation to conductivity and ionic composition.
Freshwater Biology 48: 1311–1328.
Potapova M, Charles DF. 2007. Diatom metrics for monitoring
eutrophication in rivers in the United States. Ecological Indicators
7: 48–70.
R Development Core Team. 2009. R: a language and environment
for statistical computing. Vienna: R Foundation for Statistical
Computing.
Shannon CE, Weaver W. 1949. The mathematical theory of
communication. Urbana: University of Illinois Press.
Stanford JA, Ward JV. 1988. The hyporheic habitat of river ecosystems. Nature 335: 64–66.
Stevenson RJ. 1997. Scale-dependent determinants and consequences of benthic algal heterogeneity. Journal of the North
American Benthological Society 16: 248–262.
Stoermer EF, Smol JP. 1999. The diatoms: applications for the environmental and earth sciences. Cambridge: Cambridge University Press.
ter Braak CJF. 1986. Canonical correspondence analysis: a new
eigenvector technique for multivariate direct gradient analysis.
Ecology 67: 1167–1179.
ter Braak CJF, Verdonschot P. 1995. Canonical correspondence
analysis and related multivariate methods in aquatic ecology.
Aquatic Science 57: 255–289.
Thioulouse J, Chessel D, Dolédec S, Olivier JM. 1997. ADE-4: a
multivariate analysis and graphical display software. Statistics
and Computing 7: 75–83.
Thioulouse J, Dray S. 2007. Interactive multivariate data analysis in
R with the ade4 and ade4TkGUI packages. Journal of Statistical
Software 22: 1–14.
Tison J, Giraudel JL, Park YS, Coste M, Delmas F. 2005. Classification of stream diatom communities using a self-organising map.
In: Lek S, Scardi M, Verdonschot PFM, Descy JP, Park YS (eds),
Modelling community structure in freshwater ecosystems. Berlin:
Springer. pp 304–316.
van Dam H, Mertens A, Sinkeldam J. 1994. A coded checklist
and ecological indicator values of freshwater diatoms from the
Netherlands. Aquatic Ecology 28: 117–133.
Received 21 March 2011, accepted 23 August 2011
African Journal of Aquatic Science 2012, 37(1): 59–69
67
Appendix 1: Abbreviations and names of diatom species identified from the 14 samples
Code
AACU
ACAF
ADEG
ADEU
ADLA
ADMI
ADPY
ADSA
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
AEXI
AINA
AMII
APED
AUGR
BNEO
BPAX
CAEX
CAFF
CBNA
CDUB
CELL
CEUG
CMEN
COCE
CPED
CPLA
CPLI
CSOL
CTPU
CTUM
DELL
DMES
DMON
DOBL
DPST
DVUL
EARC
EIMP
EINC
ENCM
ENNG
ESBM
ESLE
ESUM
FCVA
FPYG
GAFF
GEXL
GGRA
GMIN
GOLI
GPAR
GPRO
GPUM
GYAC
HHUN
HVEN
LGOE
MALC
MPMI
Name
Amphora acutiuscula Kützing
Achnanthidium affine (Grunow) Czarnecki
Achnanthidium exiguum (Grunow) Czarnecki
Achnanthidium eutrophilum (Lange-Bertalot) Lange-Bertalot
Achnanthidium latecephalum Kobayasi
Achnanthidium minutissimum (Kützing) Czarnecki
Achnanthidium pyrenaicum (Hustedt) Kobayasi
Achnanthidium saprophilum (Kobayasi & Mayama) Round &
Bukhtiyarova
Achnanthes exilis Kützing
Amphora inariensis Krammer
Achnanthidium minutissimum (Kützing) Czarnecki var.
inconspicua Oestrup
Amphora pediculus (Kützing) Grunow
Aulacoseira granulata (Ehrenberg) Simonsen
Brachysira neoexilis Lange-Bertalot
Bacillaria paxillifera (O.F.Müller) Hendey var. paxillifera
Cymbella excisa Kützing var. excisa
Cymbella affinis Kützing var. affinis
Cymbopleura naviculiformis (Auerswald) Krammer var. naviculiformis
Cyclostephanos dubius (Fricke) Round
Cymatopleura elliptica (Brebisson) W.Smith var. elliptica
Cocconeis euglypta Ehrenberg
Cyclotella meneghiniana Kützing
Cyclotella ocellata Pantocsek
Cocconeis pediculus Ehrenberg
Cocconeis placentula Ehrenberg var. placentula
Cocconeis placentula Ehrenberg var.lineata (Ehrenberg) Van Heurck
Cymatopleura solea (Brebisson in Breb. & Godey) W.Smith var. solea
Ctenophora pulchella (Ralfs ex Kütz.) Williams & Round
Cymbella tumida (Brebisson) Van Heurck
Diploneis elliptica (Kützing) Cleve
Diatoma mesodon (Ehrenberg) Kützing
Diatoma moniliformis Kützing
Diploneis oblongella (Naegeli) Cleve-Euler
Discostella pseudostelligera (Hustedt) Houk & Klee
Diatoma vulgaris Bory
Eunotia arcus Ehrenberg var. arcus
Eunotia implicata Nörpel, Lange-Bertalot & Alles
Eunotia incisa Gregory var. incisa
Encyonopsis microcephala (Grunow) Krammer
Encyonema neogracile Krammer
Eolimna subminuscula (Manguin) Moser, Lange-Bertalot & Metzeltin
Encyonema silesiacum (Bleisch in Rabh.) D.G.Mann
Encyonopsis subminuta Krammer & Reichardt
Fragilaria capucina Desmazieres var. vaucheriae (Kützing)
Lange-Bertalot
Fallacia pygmaea (Kützing) Stickle & Mann subsp. pygmaea
Lange-Bertalot
Gomphonema affine Kützing
Gomphonema exilissimum (Grunow) Lange-Bertalot & Reichardt
Gomphonema gracile Ehrenberg
Gomphonema minutum (Agardh) f. minutum
Gomphonema olivaceum (Hornemann) Brébisson var. olivaceum
Gomphonema parvulum (Kützing) Kützing var. parvulum f. parvulum
Gomphonema productum (Grunow) Lange-Bertalot & Reichardt
Gomphonema pumilum (Grunow) Reichardt & Lange-Bertalot
Gyrosigma acuminatum (Kützing) Rabenhorst
Hippodonta hungarica (Grunow) Lange-Bertalot, Metzeltin & Witkowski
Halamphora veneta (Kützing) Levkov
Luticola goeppertiana (Bleisch in Rabenhorst) D.G.Mann
Mayamaea alcimonica (E.Reichardt) Monnier & Ector
Mayamaea permitis (Hustedt) Bruder & Medlin
Code
Name
MVAR Melosira varians Agardh
NAAM Navicula amphiceropsis Lange-Bertalot & Rumrich
NACI Nitzschia acicularis (Kützing) W.M.Smith
NAMP Nitzschia amphibia Grunow f. amphibia
NCPL Nitzschia capitellata Hustedt in A.Schmidt et al.
NCPR Navicula capitatoradiata Germain
NCRY Navicula cryptocephala Kützing
NCTE Navicula cryptotenella Lange-Bertalot
NCTO Navicula cryptotenelloides Lange-Bertalot
NCTV Navicula caterva Hohn & Hellerman
NDES Nitzschia desertorum Hustedt
NDIS Nitzschia dissipata (Kützing) Grunow var. dissipata
NERI Navicula erifuga Lange-Bertalot
NFIC Nitzschia filiformis var. conferta (Richter) Lange-Bertalot
NFIL Nitzschia filiformis (W.M.Smith) Van Heurck var. filiformis
NGER Navicula germainii Wallace
NGES Nitzschia gessneri Hustedt
NGRE Navicula gregaria Donkin
NIAR Nitzschia archibaldii Lange-Bertalot
NIFR Nitzschia frustulum (Kützing) Grunow var. frustulum
NILA Nitzschia lacuum Lange-Bertalot
NINC Nitzschia inconspicua Grunow
NLAN Navicula lanceolata (Agardh) Ehrenberg
NMEN Navicula menisculus Schumann var. menisculus
NMIC Nitzschia microcephala Grunow in Cleve & Moller
NPAD Nitzschia palea (Kützing) W.Smith var. debilis (Kützing)
Grunow in Cleve & Grunow
NPAE Nitzschia paleacea (Grunow) Grunow in van Heurck
NPAL Nitzschia palea (Kützing) W.Smith
NRCH Navicula reichardtiana Lange-Bertalot var. reichardtiana
NRCS Navicula recens (Lange-Bertalot) Lange-Bertalot
NREC Nitzschia recta Hantzsch in Rabenhorst
NREV Nitzschia reversa W.Smith
NROS Navicula rostellata Kützing
NSHR Navicula schroeteri Meister var. schroeteri
NSLC Navicula salinicola Hustedt
NSUA Nitzschia subacicularis Hustedt in A.Schmidt et al.
NTHE Nitzschia thermaloides Hustedt
NTPT Navicula tripunctata (O.F.Müller) Bory
NUMB Nitzschia umbonata (Ehrenberg) Lange-Bertalot
NVDA Navicula vandamii Schoeman & Archibald var. vandamii
NVDS Navicula (dicta) seminulum (Grunow) Lange-Bertalot
NVEN Navicula veneta Kützing
NVIP Navicula vilaplanii (Lange-Bertalot & Sabater) Lange-Bertalo
& Sabater
NZSU Nitzschia supralitorea Lange-Bertalot
PLEV Pleurosira laevis (Ehrenberg) Compere f. laevis Ehrenberg
PLFR Planothidium frequentissimum (Lange-Bertalot) LangeBertalot
PMTC Psammothidium curtissimum (Carter) Aboal
PSBR Pseudostaurosira brevistriata (Grun. in Van Heurck)
Williams & Ro
PTEL Planothidium ellipticum (Cl.) Round & Bukhtiyarova
RABB Rhoicosphenia abbreviata (C.Agardh) Lange-Bertalot
RSIN Reimeria sinuata (Gregory) Kociolek & Stoermer
SANG Surirella angusta Kützing
SBRE Surirella brebissonii Krammer & Lange-Bertalot var. brebissonii
SEMN Sellaphora minima (Grunow) Mann
SPUP Sellaphora pupula (Kützing) Mereschkowksy
TAPI Tryblionella apiculata Gregory
TFLO Tabellaria flocculosa (Roth) Kützing
THUN Tryblionella hungarica (Grunow) D.G.Mann
UULN Ulnaria ulna (Nitzsch.) Compère
Chaïb and Tison-Rosebery
68
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
Appendix 2: Total counts of diatom species identified from seven sampling stations on the Kebir-East wadi in winter and summer 2007. See
Table 1 for site codes
Species
abbrev.
AACU
ACAF
ADEG
ADEU
ADLA
ADMI
ADPY
ADSA
AEXI
AINA
AMII
APED
AUGR
BNEO
BPAX
CAEX
CAFF
CBNA
CDUB
CELL
CEUG
CMEN
COCE
CPED
CPLA
CPLI
CSOL
CTPU
CTUM
DELL
DMES
DMON
DOBL
DPST
DVUL
EARC
EIMP
EINC
ENCM
ENNG
ESBM
ESLE
ESUM
FCVA
FPYG
GAFF
GEXL
GGRA
GMIN
GOLI
GPAR
GPRO
GPUM
GYAC
HHUN
HVEN
LGOE
MALC
MPMI
MVAR
NAAM
NACI
KeRSk
0
0
0
4
0
16
0
0
0
0
0
9
0
0
0
0
0
0
2
0
2
0
6
12
3
3
5
2
0
0
0
0
0
0
3
0
0
0
0
0
10
0
0
2
0
0
3
0
10
0
3
0
0
0
0
1
0
0
0
0
0
0
KebAs
0
0
0
0
0
304
0
8
0
0
0
0
0
3
0
0
0
0
0
0
0
0
63
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
1
0
1
0
6
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Summer
KebAK KebGrg KebAn
0
0
0
0
0
0
0
2
1
7
4
9
0
0
0
13
68
3
0
0
0
0
2
0
0
0
0
0
1
0
0
0
0
13
10
1
0
1
1
0
0
0
0
2
0
0
2
0
1
0
0
0
0
0
0
0
0
0
0
0
1
0
0
2
2
0
3
12
0
4
2
0
2
1
0
4
3
4
2
2
0
0
0
0
0
1
12
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
2
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
7
5
1
1
1
3
0
3
0
0
0
0
1
1
0
0
0
0
1
2
0
0
0
0
2
0
0
2
1
0
7
6
7
0
0
0
1
3
1
0
0
0
0
0
0
3
0
0
2
4
10
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
KebRg
0
0
0
0
1
14
1
1
0
1
0
0
16
0
23
0
0
0
0
0
1
9
18
0
0
9
0
0
0
1
0
0
0
4
0
0
1
0
0
0
6
0
0
2
0
1
0
0
0
0
3
0
0
1
1
1
4
0
0
0
0
15
KebSb
0
2
3
21
0
55
12
5
6
0
0
1
5
0
0
0
0
0
0
0
0
0
9
0
0
1
0
0
5
0
0
0
0
1
0
1
2
0
0
2
2
4
2
0
0
0
2
0
0
0
4
0
0
0
0
0
24
0
0
0
3
3
KeRSk
0
0
0
2
1
12
0
3
0
0
1
1
0
0
1
0
1
1
0
0
0
4
6
6
0
7
0
0
0
0
0
0
0
0
1
0
0
0
0
0
15
0
0
4
0
0
2
0
3
0
6
1
2
0
0
0
1
9
0
2
7
1
KebAs
0
0
0
7
1
59
0
6
0
0
0
3
0
1
0
0
0
1
0
0
0
2
26
4
0
4
1
0
0
0
0
1
0
0
6
0
0
0
0
0
4
0
3
0
0
0
1
0
1
1
7
0
2
0
0
1
1
18
1
0
1
0
Winter
KebAK KebGrg KebAn
1
0
0
0
0
0
1
0
1
7
4
11
0
0
0
18
20
2
0
0
0
2
3
3
0
0
0
0
0
0
0
2
0
10
14
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
3
0
2
5
1
8
5
0
0
0
0
2
6
4
3
1
0
0
0
0
0
0
12
1
0
0
0
1
0
2
1
0
0
1
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
3
7
1
1
0
0
0
0
0
0
0
0
1
0
0
0
0
0
4
0
2
0
0
0
4
6
0
1
0
0
3
7
11
0
0
0
1
2
1
0
0
0
0
0
0
2
0
0
0
1
7
5
6
0
2
0
0
0
0
0
0
0
0
2
1
2
KebRg
0
0
0
3
0
9
0
0
0
0
0
10
2
0
1
1
0
0
0
0
0
2
4
2
0
4
0
0
0
0
0
0
0
2
1
0
0
0
0
0
12
0
1
0
1
0
1
0
0
1
4
0
2
0
0
1
0
19
0
0
0
2
KebSb
0
0
0
6
0
14
0
2
0
0
0
7
0
0
1
0
0
0
0
1
0
3
6
5
0
3
4
0
0
2
0
3
0
0
1
0
0
0
0
1
3
0
0
0
0
0
0
1
0
1
8
0
3
0
0
0
5
7
1
0
0
2
69
African Journal of Aquatic Science 2012, 37(1): 59–69
Downloaded by [University of Milan], [Nadjla Chaib] at 13:21 21 June 2012
Appendix 2 (cont.)
Species
abbrev.
NAMP
NCPL
NCPR
NCRY
NCTE
NCTO
NCTV
NDES
NDIS
NERI
NFIC
NFIL
NGER
NGES
NGRE
NIAR
NIFR
NILA
NINC
NLAN
NMEN
NMIC
NPAD
NPAE
NPAL
NRCH
NRCS
NREC
NREV
NROS
NSHR
NSLC
NSUA
NTHE
NTPT
NUMB
NVDA
NVDS
NVEN
NVIP
NZSU
PLEV
PLFR
PMTC
PSBR
PTEL
RABB
RSIN
SANG
SBRE
SEMN
SPUP
TAPI
TFLO
THUN
UULN
KeRSk
0
0
0
0
3
8
21
2
15
0
0
0
0
1
70
1
35
0
5
36
0
1
1
0
12
0
6
1
0
0
0
0
0
1
1
0
2
2
1
0
1
1
1
0
0
0
0
0
0
72
1
0
12
0
0
0
KebAs
0
0
0
1
0
0
0
0
2
0
11
0
0
0
0
0
2
0
0
0
0
0
0
0
6
0
2
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
Summer
KebAK KebGrg KebAn
0
1
0
0
2
0
0
3
1
7
0
0
3
0
0
8
3
0
16
11
0
0
1
4
26
9
4
0
0
0
0
41
129
0
0
0
0
0
0
0
1
0
65
24
0
0
0
0
32
62
91
0
0
0
0
0
0
31
15
0
5
0
0
0
0
0
0
0
0
0
1
0
18
5
7
1
0
0
2
12
114
0
0
0
0
0
0
4
6
1
4
2
1
0
0
0
0
0
0
0
0
0
1
1
0
0
1
0
0
0
0
0
0
4
1
0
1
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
4
7
0
0
0
1
0
0
2
0
1
0
0
0
78
39
0
0
1
7
0
0
0
14
11
0
0
0
0
1
0
0
0
1
1
KebRg
3
1
0
0
0
0
0
0
1
0
54
0
48
0
0
0
24
0
0
1
0
0
0
0
44
0
14
0
1
24
8
1
4
0
0
0
5
13
3
0
0
0
0
0
15
0
0
0
0
1
0
0
0
0
0
1
KebSb
0
0
0
0
0
0
0
0
2
2
37
3
3
0
0
0
103
8
0
0
0
0
0
0
16
0
20
0
0
4
2
0
1
0
0
0
0
8
0
0
0
0
1
6
11
0
0
0
0
0
5
0
0
0
0
1
KeRSk
0
9
1
0
3
2
7
4
7
0
7
0
0
0
87
0
37
0
0
36
0
0
0
0
14
0
4
0
0
4
3
0
0
0
1
0
0
1
0
0
0
1
0
0
6
0
1
1
0
59
0
0
6
0
0
0
KebAs
0
6
4
0
1
0
8
5
2
0
2
0
0
0
43
0
69
0
0
12
0
0
0
0
10
0
0
0
0
0
1
0
1
0
0
0
3
0
0
1
0
1
0
0
1
1
1
1
0
56
0
0
7
0
0
1
Winter
KebAK KebGrg KebAn
0
0
0
2
5
0
3
1
0
0
0
0
12
7
0
2
4
0
19
22
1
1
6
0
12
6
0
0
1
0
1
6
77
0
0
0
0
0
4
0
0
0
64
65
0
0
0
0
69
87
139
0
0
22
0
0
0
32
21
0
0
0
0
0
0
0
0
0
0
0
0
0
12
7
3
0
0
0
5
0
75
0
0
0
0
0
0
0
1
0
1
0
5
0
0
0
2
3
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
3
0
2
0
0
0
0
0
0
0
1
0
1
0
0
0
0
0
0
1
0
8
0
0
0
0
1
0
0
0
0
0
0
0
67
55
0
0
0
6
1
0
2
4
8
0
0
0
0
0
0
0
1
0
2
KebRg
0
2
3
1
3
3
21
4
7
0
3
0
0
3
60
0
113
1
0
25
0
0
0
0
14
0
6
0
0
0
2
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
0
0
36
0
0
6
0
0
0
KebSb
1
1
2
0
6
0
15
1
17
0
13
0
4
0
64
0
42
2
0
51
0
0
0
0
14
0
7
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
1
0
1
1
1
51
2
0
12
1
0
0
Téléchargement