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KH. M. A B O U - A I S H A 1, I. A. KOBBIA1, * M. S. EL A B Y A D 1,
EFFAT. E S H A B A N A l and E S C H A N Z 2
l Department of Botany, Faculty of Science, Cairo University, Egypt. 2 Institutfiir Pflanzenbiologie
limnologie, Ziirich University, Switzerland.
Abstract. This study was undertaken to investigate the impact of phosphorus loadings on the seasonal
abundance and diversity of macro-algal communities at three sites of the Egyptian coastal region of
the Red Sea. Sea-water analysis revealed no significant variations in the levels of dissolved inorganic
carbon at these sites. Nitrate content was highest during the winter season especially at Ghardaqa.
The localized phosphate pollution at the two other sites significantly increased the phosphate level in
water which led to significant decreases in biomass of the macroalgae as compared to Ghardaqa.
The intertidal zone at one of the impacted sites supported very poor algal vegetation, dominated by
Phaeophyta in winter and spring and Rhodophyta in summer and autumn; at Quseir it was dominated
by microfilamentous Rhodophya. At Ghardaqa, the intertidal macro-algal community was dominated
by Phaeophyta. The results also showed that the abundance of marcroalgae reached its maximum in
August at all the study sites, and that species diversity was significantly higher at Quseir than at the
other two sites.
1. Introduction
The Red Sea has been considered one of the least-affected areas by pollution in the
world (Head, 1987). The sea is a semi-closed basin with no river inflow situated in
an arid zone where evaporation greatly exceeds precipitation (Poisson et al., 1984).
Many areas of the sea have been impacted by natural catastrophes (Loya, 1976).
Pollution induced by anthropogenic activities including oil spills and excessive
loading of nutrients through addition of fertilizers and industrial waste water and
sewage have been reported (Mergner, 1984).
There are two major sources of nutrients avail to the sea, firstly, sewage outfalls,
and secondly, the escape of phosphate dust during the loading of crushed phosphate
rocks onto ships or railway wagons exacerbated by the prevailing northerly winds.
It is worth noting that no industrial waste avail in the studied area. Numerous
studies, mainly taxonomic, had already been done with marine algae in the Red
Sea (e.g. Nasr, 1947; Papenfuss, 1968). However, studies which deal with the
quantitative aspects of the standing crops of algae or the Red Sea coral reefs are
lacking.
* Corresponding author.
". i
E ilotj~ . . . . ...... ..
Sinai
0 50 100 Krn
L R t t I
Scale
Ghardaqa ~o
27 ~ _
c~
Safaga ~o
o o o~
o
26 - - Quseir ~o ~0
EGYPT %
2r I I \1 1
Fig. 1. M a p of the northern Red Sea showing the three study sites at Ghardaqa, Safaga and Quseir
(e), and the localities from which the samples were collected (o).
Ghardaqa (Hurghada), Safaga and Quseir are located at the Egyptian Red Sea
coast (Figure 1). The presence of a continuous reef fiat was used as a criterion in
IMPACT OF PHOSPHORUSLOADINGS 287
choosing the collection stations at the three study localities. The sea shores of these
regions are backed by an arid, high-mountain zone (1200-2100 m) bounding the
rift valley and separated from the sea by about 15 km of undulating plain formed
of sedimentary rock covered with black gravel. The actual coastline, as is almost
invariably the case for the Red Sea, is a raised coral reef which is generally, fronted
by a steep upper fore-reef zone. In most areas these raised coral cliffs are often
undercut by wave action, which also cuts reef platforms extending southwards
to terminate in vigorously growing fringing reefs. Sampling was carried out on
the following dates in order to cover all seasons: 17-21 February; 19-21 May;
20-22 August; and 5-7 November, 1985. At Ghardaqa, samples of seawater and
algae were collected at the vicinity of the Marine Biological Station, situated at
27~ 33~ At both Safaga (latitude 26~ 33~ about 60 km from
the sampling site at Ghardaqa), and Quseir (26~ 34~ about 120km from
Ghardaqa), seaweeds were collected from sites situated approximately 1 km far
from the phosphate factories. The average minimum seawater temperature of the
study area was recorded in February (21 ~ and the maximum in August (32.2 ~
For all seawater samples, salinity levels (determined using a "LF 56 Messtechnik"
conductivity meter) were higher tlaan.40% and had an annual average of 42.7%.
At least three water samples were collected from the surface 10 cm from each
locality and the following parameters were determined in each sample. The dis-
solved 02 concentration was determined using the Winkler method as described
by Strickland and Parsons (1972). Both carbonate and bicarbonate levels were
determined according to Golterman et al. (1978). Another set of seawater samples
was collected in acid-washed dark glass bottles, preserved in 1% solution of HgC12
and analysed for nitrate and phosphate concentrations following the methods of
Strickland and Parsons (1972).
For the assessment of the biomass of the different macroalgal inhabitants of the
intertidal zone, a transect approximately 100 m long and 30-40 m wide was drawn
parallel to the shoreline. The transect was subdivided into a number of surbareas
or "strata", where obvious discontinuities in the algal community were observed
(Gonor and Kemp, 1978). In each stratum, a number of 1 m 2 quadrats (mostly
1-3, according to the density of vegeation) were positioned in such a way as
to maximize the number of algal species included in the sample (Brower and
Zar, 1977). Quadrats of each stratum were pooled together and their average
algal abundances were calculated. The same sample size was determined at both
the phosphorus-polluted areas (at Safaga and Quseir) and at the control area (at
Ghardaqa). On return to the laboratory, the algae were rinsed in fresh seawater
288 KH. M. ABOU-AISHAET AL.
to wash out sediments and sorted into species, and the number of individuals of
each species was determined. For determining the numbers of macroalgal species
possessing creeping stolons and sending up upright assimilators (e.g. Caulerpa and
Turbinaria spp.) the number of fronds was determined as being the functional units
(Cousens and Huchings, 1983). In case of Jania species, only the number of more
or less spherical algal clumps was counted. The plants were then washed in fresh
water and their dry weights were determined after drying the species-samples at
80 ~ to a constant dry weight. Macroalgal identification was carried out according
to Nasr (1947), Papenfuss (1968); Papenfuss et al. (1982) and Farghaly (1980).
The general species diversity was determined using the Shannon-Weaver index H ~
(Magurran, 1988):
H! '3 9
= - - E i = I (P1 log2 pi)
where H ~ = number of bits per individual; s = no. of species; pi = Ni/N (Ni ---
biomass of individuals of species i, N = total biomass). The diversity index H ~ is
expressed in terms of average information per individual (Krebs, 1989). A jack
knifing technique (for details see Magurran, 1988) was used to improve the H ~
estimate by recalculating the overall diversity while missing out each quadrate in
turn. A two factor ANOVA was then computed to assess the regional versus the
seasonal variations in diversity.
The use of the K-dominance plots as a method for detecting the changes induced
by pollution disturbances on marine macrobenthic communities was applied as
outlined by Warwick (1986) and depicted in Figure 2.
Average levels of inorganic phosphates and nitrates obtained from the analyses
of coastal surface waters at the three study localities during the 1985 sampling
period are given in Table I. The average phosphate concentration at Ghardaqa was
0.32 g L -1 P which is very close to the value reported by Morcos (1970), for
waters flowing into the Red Sea (0.3 g L -1 P), although he reported values of 0.8 g
L-1 p for the outflowing waters. On the other hand, the average phosphate level
measured at Safaga was 0.79 g L -1 P and at Quseir was as higher (5.93 g L -1 P
equivalent to 18.2 g PO4 L - I P). Freemantle et at. (1978) studied the solubility
TABLE I
Levels of dissolved inorganic carbon (DIC) in mg L -1, nitrate and phosphate (/zg L -1) in surface seawater samples
collected at Ghardaqa, Safaga and Quseir during the 1985 sampling periods
16-20 Feb. 0.33 3.14 33.4 0.88 1.64 34.4 5.18 1.86 34.3
0
19-21 May 0.29 2.14 30.9 0.73 1.39 31.7 4.18 1.50 30.7
20-22 Aug. 0.31 1.86 30.3 0.79 0.73 31.5 5.93 0.89 30.4 t-
9
5-7 Nov. 0.32 1.95 30.7 0.75 0.75 30.3 5.31 0.85 28.3
Annual mean 0.32 2.27 31.3 0.79 1.13 32.0 5.16 1.27 31.0
tO
',D
290 KH.M. ABOU-AISHA ET AL.
t0o-
c
E
o
o
f
o J
9 50- f
f
? 7
E Numbers
..... Biomass
i i i
5 10 s lb 5 1(I
Species rank
II Chlorophyta [ ] Phoeophytal~JRhodophyta
A
100-
8O"
6O-
z,0j
2o j
80
2 6 , ,
o| 1.0j
o 20 ~
u 0"
L
t~ ~AA
C
80
60
I I
40
Sampling date
Fig. 3. Relativeproportions of green, brownand red macroalgae(% of total biomassof all individuals)
as recorded at Ghardaqa (A), Safaga (B) and Quseir (C) during the 1985 sampling periods.
700-
BB G h a r d a q a [] Safaga [] Quoseir
600 -
,.,..
500-
o~ 400-
u 300-
D
7O
c 200-
r,
"~ 100
Sampling date
Fig. 4. Seasonal variation in the intertidal macroalgal abundance (g dry weight/m -2) at the phos-
phorus polluted coastal sites at Safaga and Quseir compared to the control site at Ghardaqa during
the 1985 sampling periods. Error bars represent 1 standard error (SE) of the mean biomass (n > 6).
sampling periods, the number of species used for the biomass determinations at
Safaga ranged between 4 in August to 14 in February. When epiphytic algal species
were included, the number ranged between 9 and 28.
The macroalgal community in Quseir was characterized by the domination of
small microfilamentous Rhodophytes, while both green and brown seaweeds were
present in lower amounts (Figure 3). The abundance of the macroalgal species in
this area increased from February to reach a maximum in August (February, 144;
May, 152; August, 189; November, 109 g dry wt. m-2; (Figure 4).
The number of species recorded at Quseir was the highest of all the three sites,
varying between 17 in May and 29 in February. When the epiphytic algal species
were included, the number of species ranged from 41 to 56.
At all three sites, macroalgal abundance in August (summer) was significantly
higher than that recorded at the other times of the year (ANOVA, P < 0.001; n=l 5).
Biomass values recorded at Ghardaqa were significantly higher than those obtained
at either Safaga or Quseir (ANOVA, P < 0.001, n=20; Figure 4).
The localized phosphate pollution occuring at Safaga and Quseir was accompa-
nied by significant decreases in the abundance (g dry wt. m -2) of the macroalgal
species compared to that recorded at the control site at Ghardaqa (Figure 3). This
decrease in algal abundance, a probable response to pollution, contradicts the
results of other studies in the Gulf of Aqaba where phosphate pollution resulted
in enhanced algal growth at Eilat (Fishelson, 1973) and in doubling of the algal
biomass at Aqaba (Walker and Ormond, 1982). The increased phosphate levels at
Safaga and Quseir were also associated with changes in the relative proportions of
the different algal phyla compared to those recorded at Ghardaqa.
The most pronounced shift in the macroalgal community structure was the
reduction in abundance of the large frondose macroalgal species belonging to
Phaeophyta (e.g. Sargassum, Cystoseira, Turbinaria, Padina and Hormophysa) in
the polluted areas. Accordingly, the low relative abundance of these algae at Safaga
and Quseir might explain the low macroalgal biomass found in those areas.
The reduction in abundance of the brown seaweeds at Safaga and Quseir was
accompanied by enhanced growth of various species of small microfilamentous
algae, which collectively formed low covers (< 5 cm in height) often known as
algal turfs. In the polluted areas, these turfs were composed of several species of
red and green algae, e.g. Spyridia filamentosa, Hypnea musciformis, H. cornuta
and H. sp. Dasyaflocculosa and Acanthophora najadiformis from the Rhodophy-
ta; and Cladophoropsis, Cladophora, Chaetomorpha, Disctyosphaeria, Ulva and
Enteromorpha from the green algae. The turf algae are opportunistic species (r-
selected) having rapid growth rates, high reproductive output volume ratios (Littler
and Littler, 1980). The high half-saturation constants of these species enable large
quantities of nutrients rapidly uptaked to statisfy their high nutrient demand, which
is not possible in areas of nutrient shortage (Barnes and Hughes, 1988). Howev-
er, in contrast to the large frondose macroalgal forms, these algal species do not
contribute significantly to the total biomass (g dry wt. m-2).
294 KH. M. ABOU-AISHAET AL.
"6 5.0
_= 4 . 0
-"-r 3 , 0
'~ 2 . 0
L
|
~3 1 .o
0.0 !
1 6 - 2 0 Feb. 19-21 Moy 20-22 Aug, 5-7 Nov.
Sampling d a t e
Fig. 5. Combined K-dominance curves for biomass (dashed lines) and numbers of individuals
(continuous lines) of macroalgal species recorded at Ghardaqa (A), Safaga (B) and Quseir (C) during
the 1985 sampling periods. The percentage cumulative dominance (linear scale on the Y-axis) is
plotted against the species rank numb'er, ranked in order from most abundant to least abundant
species (logarithmic scale on the X-axis).
The K-dominance curves which illustrate the distribution of the biomass and
the total number of the individuals at Ghardaqa, Safaga and Quseir are given in
Figure 5).
At Ghardaqa the biomass was dominated by one or a few large species (belong-
ing usually to the Phaeophyta), each represented by rather few individuals. On the
other hand, the distribution of the number of individuals among species is more
even than the distribution of the biomass, which shows a strong dominance. Under
such circumstances, the curve of the biomass lies above the numbers curve, indi-
cating higher "number diversity" than "biomass diversity" (Warwick, 1986).
At Safaga, and more noticeably at Quseir, the numbers curve lies above the
biomass curve, indicating that the benthic community becomes numerically dom-
inated by small species (in this case, microfilamentous turf algae), and that few
larger species are present. Consequently, the "biomass diversity" is higher than the
"numbers diversity".
Our data show that the enhanced phosphorus concentrations at Safaga and Quseir
have affected the macroalgal species composition as well as the relative abundance
of the species which might be reflected on the diversity index. The utility of the
consept of diversity index as a measure of the pollutional status of an aquatic
IMPACT OF PHOSPHORUS LOADINGS 295
system has been recommended (Wu and Suen, 1985). In general, the reduction in
number of species and increase in number of individuals that characterizes polluted
areas would result in significant decreases in values of diversity.
The intertidal macroalgal Shannon-Weaver diversity index H ~ showed signifi-
cant seasonal and spatial variations among the three study localities (Figure 6). The
seasonal variation in H ~suggests that other factors, such as water temperature, light
intensity and grazing activity, interacted with the nutrient availability to determine
the macroalgal distribution pattern, but this needs further investigations.
A linear correlation between diversity and the level of phosphorus pollutants
in seawater at Quseir, particularly in November and February, was apparent (Fig-
ure 6). This observation fits with other studies reporting decline in diversity fol-
lowing the release of pollutants (Rai et al., 1981; Gaur and Kumar, 1986). The
macroalgal diversity in February was significantly higher than that in the other
months (ANOVA, P < 0.01; n=15). Differences in H ~values between May, August
and November were not significant (P > 0.05). The average diversity determined
for Quseir (3.65) was significantly higher (ANOCA; P < 0.05, n=20) than that
recorded for Ghardaqa (2.85) or Safaga. Differences in H ~ between Ghardaqa and
Safaga were not significant (P > 0.05).
The mean diversity at Quseir was significantly higher than that at the control
locality of Ghardaqa. This disagrees with the general assumption that species
diversity decreases following the pollution-induced perturbation of a community
(Gonor and Kemp, 1978; Magurran, 1988). This hypothesis is based on the fact that
less pollution results in dominance of a single sensitive species, while most other
species are severely reduced in number, resulting in reduced diversity. Nevertheless,
an increase in diversity may occur when a dominant species is affected by this
pollution. A reduction of the dominant's density occurs allowing other species to
increase in number (Gonor and Kemp, 1978). This latter explanation agrees with
the situation found in this study.
The removal of the competitive macroalgal dominants (perennial Phaeophytes)
and colonization with ephemeral and fugitive tuff algal species manifested itself in
the higher diversities observed.
Ogawa and Ichimura (1984) studied the changes in phytoplankton diversity
index as a function of the tropic status in 23 different inland water bodies. They
found high diversity to be associated with mesotrophic or slightly eutrophic waters,
whereas low diversity was found to be associated with oligotrophic or highly
eutrophic waters. It is suggested that the oligotrophic Res Sea waters at Ghardaqa
harbour suport a less diverse macroalgal community than the eutrophic waters at
Quseir.
In conclusion, the localized phosphate pollution at Safaga and Wuseir signifi-
cantly increased the phosphate level in water which led to significant decrease in the
biomass of the macroalgae when compared to Ghardaqa (unpolluted site). Results
of this investigation also showed that the abundance of macroalgae reached its max-
t,~
~D
February May August November c~
A
100-
100- f 100-
50 50J 50-
Q; >
._> 9
........ , , - ...... ~ 0 OI ........
10 1 10 >
-~ I 10 100 10 100
E c >
Fig. 6 .The Shannon-Weaver diversity index (H') at the three sites investigated during the 1985 sampling periods. Error bars represent one standard
deviation (SD) of the mean diversity, n=5.
IMPACT OF PHOSPHORUS LOADINGS 297
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