INTERTIDAL ALGAL SPECIES DIVERSITY AND THE EFFECT OF POLLUTION

[Manuscript received 3 July 19721

Abstract

The species diversity of the larger intertidal algae was determined at three sites along the coastline of Sydney, New South Wales. The changes in species diversity and species composition were correlated with height from mean of low water (MLW), distance from the edge of the rock platform at MLW, and distance from a sewer outfall (i.e. the degree of pollution). The total number of algal species was reduced in the vicinity of the outfall. This reduction was most evident in the Phaeophyceae and the Rhodophyceae. The maximum value of algal species diversity was also reduced at higher levels above MLW, away from the edge of the platform and near the outfalls.

In recent years the use of community parameters has become an important aspect of the study of the effects of pollution on aquatic life, both freshwater and marine (Olsen and Burgess 1967; Jenkins 1969). Among these the determination of species diversity, based on one or more trophic levels, has been used in attempts to assess water quality. Some of the communities studied so far are benthic invertebrates (Wilhm and Dorris 1966; Storrs et al. 1969), foraminifera (Bandy, Ingle, and Resig 1964), and fish (Bechtel and Copeland 1970). Prior to the present study, benthic algal populations have not been studied in this way.

Studies on the benthos have the greatest potential for revealing the cumulative effects of pollution on the marine biota. Attached algae, because of their sedentary nature, tend to integrate the effects of long-term exposure to adverse conditions. As benthic algae represent a major part of the lowest trophic level, anything affecting them must also influence organisms of higher trophic levels.

This study is an attempt to measure the species diversity of algae growing in the intertidal zone, and the changes in diversity associated with the presence of a sewer outfall.

(a) Description of Site This study was carried out on 20 km of the coastline of Sydney from North Head to Hole in

the Wall (Fig. l(a)), during the period of January to October 1970. The coastline here is directly exposed to the South Pacific Ocean and consists of alternate sandstone headlands and sandy beaches. At North Head, Sydney's second largest sewer outfall discharges about 70 million gallons of screened domestic sewage per day. Two outfall pipes discharge a few meters below mean of low water (MLW) and about 3 m away from the edge of the platform. Most of the mixing of the sewage with the sea- water occurs by wave action, which is usually very strong at the outfall.

* School of Biological Sciences, Botany Building, University of Sydney, N.S.W. 2006.

Aust. J. mar. Freshwat. Res., 1972, 23, 73-84

74 M. A. BOROWITZKA

The coastline has a normal southward flowing current of an average speed of 1 knot. However, the sewage field travels initially in a northerly direction as a consequence of a system of eddy currents induced by a long reef. Further details as to the spread of the polluted water are reported by Flynn and Thistlethwayte (1964).

Permanent transects of varying length were laid out on rock platforms at North Head (TI-T,) (Fig, l(b)), Harbord (HI, H2), and Hole in the Wall (H01, H02) (Fig. l(a)). All transects were selected for their similarity in topography and aspect, and were laid out at right angles to the edge of the platform.

Long R e d

Harbord

North Head Out fa l l r

Fig. 1 .-(a) The coastline of Sydney from Botany Bay to Broken Bay illustrating the position of the major sewer outfalls and the study sites. (b) Sketch of the platform at Bluefish Point, North Head, showing the position of the transects and the relative position] of the various regions of algal communities. x , position of the outfall pipes. (Scale is approximate.)

(b) Water Analyses The concentrations of coliform bacteria, nitrate and nitrite, and salinity were determined in

water samples collected at the various sites throughout the course of this study. Nitrate and nitrite concentrations and the number of coliform bacteria were measured according to the methods of Strickland and Parsons (1965). Salinities were determined by the CSIRO Division of Fisheries and Oceanography.

(c) Algal Growth Colonization and regrowth was observed after denuding 1 m2 areas of the substrate and

sterilizing the bare rock with a blowtorch. Specimens of all algal species present were collected for identification on all the platforms.

ALGAL SPECIES DIVERSITY AND POLLUTION 75

(d) Species Diversity Measurement

Species diversity was measured by placing a 50 by 50 cm square grid to one side of the transect line. The grid consisted of intersecting nylon lines every 5 cm. A pin was dropped at the intersection of these lines, and the presence or absence, and species of the base of the algal thallus touched by the pin, were recorded. Each grid thus gave 121 points from which the algal species diversity (ASD) was calculated. The size of the grid was chosen so that any increase in sample size did not result in a further increase in the calculated diversity.

Species diversity was calculated according to the Shannon-Weaver (1949) formula:

where pi is the proportion of the ith species in the collection. H' is the diversity of a theoretically infinite population. To estimate H' from a sample of a population, such as the attached algae of a rock platform, it must be calculated by

where Nt is the number of individuals in the ith species and N the total number of individuals in the sample (Pielou 1966, 1969). Because natural logarithms were used in the computation, the diversity units are expressed as natural bels/individual (Good 1950). As diversity indices calculated with the H equation approximate normal distribution (Bechtel and Copeland 1970), statistics based on the normal distribution can be used.

Linear and non-linear regression analyses and correlation analyses were carried out, using a Fortran programme, which was kindly supplied by Mr L. N. Balaam of the Department of Biometry, University of Sydney.

111. RESULTS

(a) Water Anabses

The mean salinity at the various sites was 35.41%,. At the outfalls a minimum value of 34.64%, was reached. The concentration of nitrate ranged from a maximum 8.6 pg-atoms N/1. to a minimum of 1 -5 pg-atoms N/1. The concentration of nitrite ranged from a maximum of 4.8 pg-atoms N/1. to an absence of nitrite. The highest values were recorded in the samples collected at the outfall; these, however, varied considerably. Mixing occurs almost immediately, and the levels of nitrate and nitrite recorded at the other sampling sites remained consistantly low. The coliform bacteria counts indicated periodic spreading of the effluent as far as Harbord. No coliforms were recorded at Hole in the Wall.

(b) The Flora and Fauna of the Sites

(i) Hole in the Wall

This large platform is 19.1 km north of North Head outfall (Fig. l(a)), and as indicated by the water analyses and the study of Flynn and Thistlethwayte (1964) can be considered free of pollution. The fauna is much like that described by Pope (1943) for Long Reef. The major algae present in the sublittoral are Ecklonia radiata, in the sublittoral fringe Pterocladia sp., and in the littoral Chylocladia gelidiodes, Corallina sp., Colpomenia sinuosa, stunted Sargassum sp., Ulva sp., and Padina pavonia. A total of 41 species were collected at this site (Table 1).

76 M. A. BOROWITZKA

(ii) Harbord This station was chosen as an intermediate site between the sewer outfall and

Hole in the Wall (Fig. l(a)). The flora and fauna of this platform have previously been described in part by Pope (1943), Dakin, Bennet, and Pope (1948), and Dakin (1952). The species of animal and plants are similar to those at Hole in the Wall. However, only 39 species of algae were collected here (Table 1).

(iii) North Head Outfall Area (Bluefish Point) Three basic regions of algal communities can be distinguished (Fig. l(b)).

Region 1.-This region is the farthest from the outfall and is characterized by a luxuriant growth of Ulva and Enteromorpha throughout most of the year. Some of the Ulva collected reached lengths of 50-100 cm. A distinct zone of Pterocladia is present, and brown and red algae are common. The coralline red algae are particularly common in pools. The fauna is similar to that at Harbord and Hole in the Wall. The tube worm Galeolaria, the sea urchin Heliocidaris, and the black elephant snail Scutus antipodes are obvious members of the fauna.

TABLE 1 TOTAL NUMBER OF SPECIES COLLECTED, AND THEIR DISTRIBUTION AMONG THE VARIOUS PHYLA

North Head in Harbord , JL the Wall 7 Total

Region 1 Region 2 Region 3 Outfall

Chlorophyceae 7 10 7 5 4 2 11 Rhodophyceae 14 13 16 9 2 0 18 Phaeophyceae 20 16 5 1 0 0 22

Total 41 39 28 15 6 2 51

Region 2.-This is the intermediate stage between the heavily polluted Region 3 and the least polluted Region 1. A Pterocladia zone is still present; the plants, however, are extremely stunted. The only Phaeophycean alga growing in this region is Ilea fascia. The fauna is also diminished, consisting of some barnacles and a few individuals of Haliotis sp. in a pool.

Region 3.-This is the zone continuously subject to pollution. Few species of algae are present here and the area is characterized by a short dense mat mainly of immature individuals of Enteromorpha and Chaetomorpha. The mat also contains many epiphytic fungi and diatoms. Near the edge of this region and Region 2 very immature and stunted Pterocladia grows, and in the spring small individuals of Bangia (?) grow above the other algae.

Right behind the outfall the mat can be considered to consist only of two species of green algae, and here there is also a total absence of animal life. Somewhat farther away the mat contains some small crustaceans and is also grazed by the periwinkle Melarapha unifasciata. The most striking feature of this region is the total absence of any zonation, the mat being of uniform structure from the sublittoral zone to the limit of algal growth.

ALGAL SPECIES DIVERSITY AND POLLUTION 77

Table 1 illustrates the reduction in species number due to increasing pollution. Particularly striking is the early total disappearance of the Phaeophyceae and the later disappearance of the Rhodophyceae. The number of species of Lhe Chlorophyceae are also reduced from 10 to two species.

TABLE 2 A LIST OF THE SPECIES AND THEIR APPROXIMATE ABUNDANCE, RECORDED DURING SAMPLING AT EACH OF

THE TRANSECTS

The transects are arranged in order of decreasing distance from the outfall. x x X , Species occurring in > 50% of the grids; x X, species occurring in 20-50% of the grids; X, species occurring in < 20% of the grids; 0, species recorded only once; ( ), species found to be markedly seasonal

Species 1 H2 I HO1 H02 I TI I T2 T5 / T4 T3

Ulva sp. Enteromorpha spp. Chaetomorpha area Codium spongiosum Codium lucasii

Ilea fascia Colpomenia sinusa Pockockiella variegatus Padina paviona Dictyota dichtona Sargassum sp. (a) Sargassum sp. (b) Ectocarpus sp.

Corallina sp. Amphiroa sp. Jania sp. Lithothamnion sp. ? Laurencia sp. Polysiphonia sp. Pterocladia pinnata Porphyra columbina Gracillaria confervoides Chylocladia gelidioides Ceramium spp. Centroceras clavatum Rhodymenia australia ? Bangia sp.* Grateloupia filiciena ?

X X X

( X I - X

X

X

X X X

X X

X

X

X X X

X X

0

X X X X X X

X

X X

X - X X X X X

X X

X X X X

(XI ( X I 0 0 X 0 X X

X X - - - - - 0

Chlorophyta

- * Probably Bangia fuscupurpurea.

Table 2 is a list of the species recorded at each of the transects, together with their approximate abundance, but does not include those algae collected elsewhere on the platform. The differential sensitivity to pollution by the different algal phyla, as illustrated by Tables 1 and 2, has also been recorded by Alfimov (1959) in the south-eastern Crimea and by Ghirardelli and Pignatti (1968) in the Adriatic Sea.

- x x x X X X

X X

(XI - X

X

X X X X X X

( x ) ( x > - - - - - -

Phaeophyta

X X X X X X

( X I - x - - - x - - -

X X X

( x ) X X

( x > -

- X X X

X X

0 0

X X X

X -

0 - - - X - 0 - - -

- X X X

x - - - - - - - - - x - - - - x - - - - - - - - - - - - - -

X x - - -

78 M. A. BOROWITZKA

Regrowth in the denuded areas at the various sites gave interesting results. All the denuded areas had a slight growth of green algae (mainly Enteromorpha) and some diatoms within a few weeks. Within 2 months the denuded squares behind the outfalls were again covered by an algal mat indistinguishable from that surrounding them. The denuded squares at transect T1 and at Hole in the Wall were at this stage covered with a thick growth of Enteromorpha and Ulva. After 5 months red and brown algae had appeared. After 12 months these cleared squares had become indistinguishable from the surrounding areas. This indicates that the algal mat behind the outfalls is an immature, pioneering community while the communities at transect TI, Harbord, and Hole in the Wall can be considered mature.

Fig. 2.-The calculated regression plane of algal species diversity versus distance from the edge of the platform at MLW (DE) and distance from the outfall (DO). Y axis, ASD (natural bels/individual); XI axis, DO (km);

X2 axis, DE (m).

(c) Algal Species Diversity

At the outfalls the algae form a fine mat of intertwining filaments, and it is impossible to measure the diversity under these conditions. However, as this mat is made up of only two species, the maximum diversity can be calculated. Maximum diversity is achieved when all species are equally abundant. For two species H",,, = 0.6932. However, the diversity was probably much less as both species were not equally abundant.

Away from the outfall towards the less polluted areas the maximum diversity recorded at each of the transects is 1.33 for transect T5, 1.05 for transect T2, 1.63 for transect T1, 1.80 and 1.12 for transects H1 and H2 respectively, and 1.90 and 2.17 for transects H01 and H02 (Table 3). There is an increase in ASD as the distance from the outfall increases. However, there is also a change in diversity associated with

ALGAL SPECIES DIVERSITY AND POLLUTION 79

with the zonation of algae on the rock platform (Fig. 2). For instance, at H 0 2 there is an initial rise in diversity away from the upper littoral towards the lower littoral zone (Table 3). After a maximum value has been reached the ASD then drops near the sublittoral zone. The presence of pools and fissures in the rocks introduces further complications. The vicinity of these semi-permanent bodies of water allows a more diverse flora to develop.

The results of the linear regression analyses are presented in Table 3. All the regressions of ASD versus any of the three parameters measured give regressions which are significant at the 1 % level. The correlation of ASD against height from MLW (Ht) and the distance from the edge of the platform at MLW (DE) is 0.5487. This result indicates that ASD is correlated with the gradient of exposure to those environ- mental factors such as wave action and desiccation, the result of which is the dis- tinctive algal zonation on rocky intertidal shores (Womersley and Edmonds 1952).

TABLE 3 RESULTS OF CORRELATION AND REGRESSION ANALYSIS OF ASD DATA

Regression Correln. F Coeff. Coeff. @.FJ

ASD versus height above MLW (Ht) ASD versus dist. from edge of platform (DE) ASD versus distance from outfalls (DO) ASD versus Ht and DE

ASD versus DE and DO

ASD versus Ht and DO

ASD versus Ht, DE, and DO

ASD versus DE and DO (Sept. 1970 data only)

** F value significant at the 0-1 % level; * significant at 1 % level.

Algal species diversity becomes less as the amount of stress (e.g. dehydration, wave action, length of duration of emersion) increases. The correlation of 0.6991 of ASD against distance from the edge of the platform (DE) and distance from the outfall (DO) illustrates the influence of the gradient of pollution upon the ASD. It is the combination of the degree of exposure and the degree of the pollution of the water which is most significant in determining the type and diversity of algal community that is established. The calculated regression plane is of the form

ASD = 1 a247-0.054HtfO.040DO.

This equation is significant at a probability less than 0.001. The regression plane represented by this equation is illustrated in Figure 2. The Height from MLW is not

80 M. A. BOROWITZKA

as important in the determining the ASD as the distance from the edge of the platform and the distance from the outfall. The addition of this variable in calculating the regression and correlation actually reduces the F value slightly. This is probably due to the topography of the transects selected. All the transects were fairly flat and only had a slight upward gradient away from the sea.

As a curvilinear model, an asymptotic curve was used in one or more dimensions. None of the regressions calculated using this model gave a fit as good as the linear model. The use of a different model or more data might produce a better fit. The linear model used does give a good approximation to the real situation. However, there is some degree of error, particularly in the region of low diversity at the outfall.

IV. DISCUSSION

(a) Changes in Species Composition

As shown in Tables 1 and 2 one of the effects of pollution is to reduce the number of species of algae, particularly those of the Phaeophyceae and the Rhodophyceae. The suggestion that the brown algae are particularly sensitive to the dilution of seawater (Den Hartog 1959) is not applicable here as the changes in salinity are less than 2%,, a change which does not affect the littoral algae which are very resistant to osmotic changes (Biebl 1938; Ried 1969). Changes in the intensity of grazing due to the reduction in the numbers of herbivores as a result of the pollution, cannot account for the great differences in species number. May, Bennet, and Thompson (1970) have shown that the absence of grazers resulted only in an increase in the populations of Ulva.

Growth experiments with unicellular algae and with Ulva indicated that nitrates were one of the limiting nutrients (Borowitzka 1970). Phosphates were not limiting. Rhyther and Dunstan (1971) also found that nitrogen is the "critical limiting factor" for planktonic algal growth in the coastal region of the east coast of America.

Other components of the sewage released at North Head are detergents and greases. Of the land-derived phosphates in coastal waters, 25-50 % can be attributed to detergents (Ferguson 1968). The added nitrates and phosphates probably favour the growth of algae, particularly the greens (Nasr and Aleem 1948; Waite 1969). Detergents also contain surfactants. These affect the permeability of cell membranes (Hotchkiss 1946), and they have also been found to be toxic to some algae (Boney 1968). Nothing is known about the effects of greases on algal growth. Much of the particulate matter in the water near the outfalls settles on the surface of the algal thalli, reducing the amount of light incident upon the chloroplasts and thereby reducing the photosynthetic rate.

The reduction in the numbers of species of browns and reds may well be a result of the toxic effects of the detergents and other unknown components of the sewage, together with the increase in nutrients favouring the growth and development of the green algae, particularly Ulva and Enteromorpha (Cotton 1910; Nasr and Aleem 1948; Grenager 1957; Den Hartog 1959). The ability of Ulva and Enteromorpha to survive in polluted areas is probably also due to the great reproductive capacity of these algae and to their rapid growth rate. This enables the algae to recolonize the more polluted regions even after most of the population is killed by periodically

ALGAL SPECIES DIVERSITY AND POLLUTION 81

extreme conditions. The decrease in the number of grazers in the vicinity of the outfall would also favour colonization and regrowth.

TABLE 4 SPECIES DIVERSITY DATA

Transect* species A'ga1 Ht DE DO and date diversity (m) (m) (km>

TB (June) 0.6932t 0-2.4 0-15 0.0

T4 0.6932t 0-3.0 0-19 0.0

T,$ (June) 1.33 1.70 0.5 0.05 1.23 1.82 2.3 0.05 0.36 2.30 5.0 0.05

(Aug.) 0.75 1.82 2.3 0.05 0.60 2.30 4.7 0.05

T2 (June) 1.05 1.02 0.5 0.06 0.65 0.85 1.0 0.06

Transect* A'ga' Ht DE DO species

and date diversity (m) (m) (km)

H02 (Sept.) 1.72 1.43 4.0 19.1 2.17 1.43 7.0 19.1 1.59 1.43 9.0 19.1 1.38 1.43 17.0 19.1 1.01 1.38 20.0 19.1 0.55 1.30 23.0 19.1 0.49 1.23 26.0 19.1

* Transects TI-T, at North Head, Transects H1 and H2 at Harbord, and Transects H01 and H 0 2 at Hole in the Wall.

t Maximum estimate (see text). $ Between the two outfalls (see Fig. l(b)).

82 M. A. BOROWITZKA

(b) Species Diversity

Phytoplankton populations reach maximum values of species diversity of 4.0-6.0 (Ewing and Dorris 1970; Edden 1971). This study shows that the species diversity of the communities of the attached macrophytes of the intertidal rock platform is much lower than this. These algal communities exist in an unstable environment subject to great environmental stresses such as desiccation, drastic osmotic changes, and wave action. These communities are an example of Sanders's (1968) "physically controlled" communities, in which adaptations are primarily to the physical environment.

The results show that there is a unidirectional trend in diversity in space along the stress or stability gradients of the environment (Fig. 2, Table 4). The decreasing harshness and increasing stability of the environment from the eulittoral towards the sublittoral result in an increase in ASD. The increase in harshness and in the instability of the environment nearer to the outfalls results in a decrease in ASD.

The results of the regrowth experiments show that the low diversity communities behind the outfall can be considered to be pioneer communities. The instability of the environment in these regions, which is due to the presence of the sewer outfalls which discharge a large volume of effluent of varied composition, hold these algal communities at this primitive, "pioneering" stage, characterized by a low ASD. The algal communities of the other regions on the North Head platform can be considered to represent a gradient of communities from pioneer to relatively mature. The gradient of stress and instability, resulting from the presence of the outfalls, holds these communities at their respective stages of maturity.

The results show that with increasing pollution there is a decrease in the number of species of algae and also a reduction in algal species diversity, and that it is possible to measure this change in ASD due to pollution some distance from the source of pollution. As the ASD is also affected by other factors of the environment such as the degree of exposure of the algae and the other factors associated with algal zonation, a large number of measurements of ASD must be made, and the appropriate statistical analyses carried out to isolate the causal factors. More work needs to be carried out to determine which components of the effluent cause these changes in diversity.

This work was carried out as part of the requirement for the degree of Bachelor of Science with Honours at Sydney University.

I wish to thank Dr A. W. D. Larkum for his advice and help throughout all aspects of this work. I would also like to thank Dr P. J. Meyerscough and Dr H. F. Recher for some interesting discussions and their comments on a number of aspects of this study, and Mr R. R. Antill who provided much needed help with the field work.

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