Estuarine, Coastal and Shelf Science 61 (2004) 331–338

www.elsevier.com/locate/ECSS

Periphyton indicate effects of wastewater discharge in the

near-coastal zone, Perth (Western Australia)
Jeffrey Cosgrovea,*, Di Walkera,1, Peter Morrisonb, Karen Hillmanc,2
a
Botany Department, Faculty of Science, University of Western Australia, Hackett Drv., Crawley WA 6009, Australia
b
Sinclair Knight Merz Pty. Ltd., PO Box H615., Perth WA 6000, Australia
c
D.A. Lord & Associates Pty. Ltd., PO Box 3172 Broadway, Nedlands WA 6009, Australia
Received 2 September 2003; accepted 27 May 2004

Abstract

Periphyton communities on artificial substrata were successfully utilised as a biological indicator of the potential eutrophic effects
of wastewater discharge into coastal waters off Perth, Western Australia. Biomass and percentage carbonate content measurements
of periphyton communities grown in situ indicated that the periphyton primary production (organic weight) was enhanced in the
vicinity of the discharge outlets, with a significant negative correlation between distance north of the northern outlet in Whitfords
Lagoon and periphyton organic weight (OW) observed in autumn at a depth of 4 m (r Z ÿ0.704, P ! 0.001). However, this
response was primarily limited to the relatively calm autumn season and substrata at depths of 2 m and 4 m. Thus, in favourable
conditions phytoplankton and high relief reef communities are more likely to exhibit a eutrophic influence (in the form of enhanced
primary production) of the treated wastewater discharge. Laboratory studies confirmed that treated wastewater, diluted 100-fold to
estimate surface concentrations above the wastewater outfalls in the field, stimulates periphyton growth above levels recorded in
unpolluted seawater (F Z 12.485; P Z 0.0073).
Ó 2004 Elsevier Ltd. All rights reserved.

Keywords: periphyton; wastewater; eutrophication; artificial substrata; Perth coastal waters

1. Introduction 46% of the estuarine surface area in the United States is

impacted by nutrients (Lewis et al., 2002a).
Eutrophication has the potential to be a severe In Western Australia, concern for the ecological
environmental problem in coastal and estuarine waters integrity of the oligotrophic coastal waters adjacent to
(Mattila and Räisänen, 1998). European coastal areas its capital city, Perth, has been heightened over the last
have experienced widespread environmental deteriora- two to three decades due to the development of eutrophic
tion due to eutrophication (Bokn et al., 2002) and about conditions in the marine embayment of Cockburn Sound
(Cambridge et al., 1986), the Peel-Harvey estuarine
system (Johannes et al., 1994), and to a lesser extent, the
* Corresponding author. Algal Research Group, School of Bi-
Swan-Canning estuary (Rose, pers. comm.).
ological Sciences & Biotechnology, Department of Science and Approximately 85% of Perth’s treated wastewater is
Engineering, Murdoch University, Murdoch WA 6150, Australia. discharged to the coastal region (unpublished data), pro-
E-mail address: [email protected] (J. Cosgrove). viding an estimated 50% of the new nitrogen input into
1
Present address: School of Agriculture and Biological Sciences, this zone (Thompson and Waite, 2003). Surveys of waters
Faculty of Science, University of Western Australia, Hackett Drv.,
Crawley WA 6009, Australia. surrounding two of Perth’s major coastal wastewater
2
Present address: DAL Science & Engineering Pty. Ltd., PO Box outlets have found elevated light attenuation, nutrients,
3172 Broadway, Nedlands WA 6009, Australia. and chlorophyll-a (Thompson and Waite, 2003).

0272-7714/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2004.05.008
332 J. Cosgrove et al. / Estuarine, Coastal and Shelf Science 61 (2004) 331–338

Periphyton can reflect recent environmental condi- limestone reefs, resulting in an annual median flushing
tions, and may respond to both chemical and physical time of 2 days (Lord, 2000). Wastewater characteristics
stress (Masseret et al., 1998). Studies have shown that from the treatment plant discharging into this northern
periphyton biomass increases in response to nutrient zone, and previously measured significant impacts on
enrichment in both freshwater (Fairchild et al., 1985; the surrounding water column, are described in Table 1.
Perrin et al., 1987; Pringle, 1987) and coastal environ- The plume from the outlet at Whitfords Lagoon tended
ments (Sundbäck and Snoeijs, 1991; Hillebrand and to travel north; however, on occasion there may be
Sommer, 1997, 2000a,b; Hillebrand and Kahlert, 2001; a southerly extension (Lord, 2000). Six sites were located
Bokn et al., 2002). Increased concern for the ecological at Whitfords Lagoon around the northern outlet
integrity of coastal and estuarine waters has prompted (Fig. 1A): four at increasing distances to the north
investigation into the accumulation of periphyton on (300 m, 1000 m, 2000 m and 3500 m) and two to the
artificial substrata as an indicator of water quality south (300 m, 1000 m). The closest reef community in
(Silberstein et al., 1986; Neverauskas, 1987; Mattila and this location was approximately 3800 m north of the
Räisänen, 1998; Bokn et al., 2002; Lewis et al., 2002a,b). outlet. A reference site for this area was located 2 km
The purpose of this study was to determine if south of the outlet (2000S) as this location is unaffected
periphyton grown on artificial substrata could be used by the wastewater plume or other pollution sources
as an indicator of enhanced primary production in (Sinclair Knight Merz, 2003).
Perth’s coastal waters as a result of wastewater
discharge from two large wastewater outlets. The
percentage carbonate content (%CO3) of these periph- 2.1.2. Southern outlet
yton communities was assessed as a potential indicator At the time of the study, the southern outlet
of gross change in community composition from slower discharged wastewater (primary treatment only) into
growing calcifying species to more opportunistic species the Sepia Depression at a depth of 20 m (see Table 1 for
that deposit little or no calcium carbonate. For the more information). This is a hydrodynamically active
purposes of this study periphyton is defined as ‘all of the zone with an annual median flushing time of !1 day.
autotrophic eukaryotes, other than plants, growing on The plume travels predominantly northward in summer
submerged material in the water’. and southward in winter (Lord, 2000). Three sites were
located in the Sepia Depression at increasing distances
from the southern outlet (Fig. 1B). They extended in
2. Materials and methods

2.1. Field study Table 1

Basic characteristics of the wastewater outlets, nutrient concentrations
in the effluent, and some statistically significant impacts relative to
Perth, located on the west coast of Australia at background (modified from Thompson and Waite, 2003)
31.58  S 115.49  N, is the capital of Western Australia. Southern outlet, Northern outlet,
Its coastal waters extend from Timms Thicket near Sepia Depression Whitfords Lagoon
Mandurah to the south, 120 km northwards to Yan- Length (m)a 4200 w1720
chep. Nitrogen has been identified as the limiting Depth (m)a 20 10
nutrient in Perth’s coastal waters, although phosphorus Flow (ml dayÿ1)a 101 80
may become important under certain conditions. The NO2 C NO3 (mg Lÿ1)a 0.1 26
Perth metropolitan coastal waters comprise a moderately NH4 (mg Lÿ1)a 50 4.4
TP (mg Lÿ1)a 11 8.7
energetic, subtropical oligotrophic ecosystem which is TSS (mg Lÿ1)a 113 27
exposed to the open ocean. The coastal structure is Annual mean current 0.128 (0.415) 0.086 (0.314)
complex and the near-shore area consists of a series of speed (max) (m sÿ1)b
coastal basins bounded by a dissected chain of limestone Water column stabilityc Less tendency More tendency
reefs running parallel to the shore. The dominant to stratify to stratify
Water temperaturec Slightly cooler Slightly warmer
forcing mechanism in Perth’s coastal waters is the Light attenuationc 32%
action of the wind (Pattiaratchi and Knock, 1995). PO4c 259% 301%
Study sites were located around two ocean outlets NO3c 548%
that discharge treated wastewater from wastewater NH4c 450%
SiO4c 163%
treatment plants (WWTPs) into adjacent coastal waters.
Chlorophyll-ac 221%
a
From Lord (2000).
2.1.1. Northern outlet b
Mean (maximum) measured at 7 m depth, from Pattiaratchi et al.
The northern outlet discharges wastewater (activated (1995).
secondary treatment) into Whitfords Lagoon, a shallow c
Statistically significant increases observed at outlet, relative to
location (10 m deep) with some protection from background.
 J. Cosgrove et al. / Estuarine, Coastal and Shelf Science 61 (2004) 331–338 333

Fig. 1. Map of study areas indicating site locations at (A) Whitfords Lagoon (northern WWTP) and (B) Sepia Depression (southern WWTP). Axes as
Australian arid system.

a north-easterly direction (at distances of 500 m, 1000 m most dominant (biomass) species were made. Sample
and 2000 m) towards those reefs deemed most likely to dry weight (DW), organic weight (OW) and carbonate
be impacted by the plume. A reference site was located content were determined by drying at 40  C and
4 km to the south. gravimetric loss by ashing at 550  C and 990  C,
Experimental units were constructed that allowed respectively. Carbonate content per se is not considered
three artificial substrata to be suspended in the water a useful measure of pollution; however, its value as
column, each at a different depth (2 m, 4 m and 8 m). a proportion of OW (i.e. percentage carbonate content,
Artificial substrata consisted of a lightly scoured %CO3) is considered a potentially useful indicator of
150 mm ! 150 mm ! 3 mm PVC (Poly-Vinyl Chloride) eutrophication. Faster growing species (such as Ulva sp.)
plate. Six replicate units (6 ! 3 Z 18 plates) were will become more dominant in higher nutrient envir-
deployed at each site and left for an incubation period onments (Bokn et al., 2002), out-competing slower
of 30 days. Upon collection the plates, with periphyton growing, encrusting calcareous species. Thus periphyton
still attached, were immediately placed into individual in nutrient rich marine waters tends to have lower
plastic bags and stored on ice for transport back to the %CO3 than in oligotrophic marine waters.
laboratory where they were frozen for storage until they Data were transformed, where necessary, to achieve
could be processed. normality (log10-transformation for biomass data; arc-
The sampling procedure took place in 1995 and was sine transformation for %CO3 data) and correlation
performed once in summer (February) and again in and three-way ANOVA (direction ! depth ! distance
autumn (April). The PVC plates were washed in 10% from outlet) analyses performed for each season. On
HCL between sampling periods. all occasions, assumptions for conducting an ANOVA
Periphyton was removed from each plate by scraping. were met. Post hoc tests were performed at the 0.05
General (qualitative) taxonomic observations of the significance level.
334 J. Cosgrove et al. / Estuarine, Coastal and Shelf Science 61 (2004) 331–338

2.2. Laboratory study 6.0

A. 2m
To confirm the relationship between enhanced 5.0 4m
8m
periphyton growth and wastewater, nine artificial sub-
strata were seeded for a 14-day period at reference sites 4.0

O UTLE T
and transferred to 20 L aquaria maintained at 15  C on
a 12 h/12 h (light/dark) photoperiod cycle for 6 weeks. 3.0
Previous work had indicated that a 14-day seeding
period would allow for the development of a substantial 2.0

Organic Weight (g 100cm )

-2
diatomaceous mat interspersed with germlings of
filamentous species including Polysiphonia sp., Ulva 1.0
rigida, Enteromorpha spp. and Ectocarpus siliculosus
(unpublished data). Each plate was randomly allocated 0.0
to one of three treatments (three replicates each): control 6.0

(unpolluted seawater), Northern (treated wastewater B.

taken from the northern WWTP, secondary treatment), 5.0

or Southern (treated wastewater taken from the

southern WWTP, primary treatment). Treatment plant 4.0
effluent was diluted 100-fold in order to approximate
the surface concentration of effluent directly above the 3.0
wastewater outlets (Pattiaratchi et al., 1995).
Periphyton was harvested by scraping and DW, OW 2.0
and %CO3 measured. Treatments were compared using
one-way ANOVA. 1.0

0.0
3. Results 3500N 2000N 1000N 300N 300S 1000S 2000S
*
Site
The three measured variables, DW, OW and %CO3 Fig. 2. (A) Summer and (B) autumn periphyton organic weight
indicated significant changes in periphyton growth. Due measured at sites of varying distance north and south of the Northern
to similarities between DW and OW, only OW and outlet at 2 m, 4 m, and 8 m depth. Vertical error bars indicate standard
error. *Reference site.
%CO3 results will be shown.

3.1. Organic weight

at the reference site (2000S). A similar but less sig-
3.1.1. Northern outlet nificant pattern was observed at depth of 4 m, however,
Summer data indicated that sample depth, as well as OW at 3500N was not significantly different from the
direction and distance from the outlet, had significant reference site at this depth. There was a significant
main effects (F2,97 Z 33.52, F1,97 Z 8.41 and F3,97 Z negative correlation for samples grown at 4 m between
5.86, respectively), at the 0.05 level, on periphyton OW. distance north of the outlet and OW (r Z ÿ0.704,
Tukey tests revealed that OW was significantly lower P ! 0.001). The mean OW at sites to the south of the
than the reference site at 300N and 1000N at depths of outlet was not significantly different from the reference
4 m and 2 m, respectively (Fig. 2A). site at any depth (Fig. 2B).
Autumn data indicated that sample depth, as well as Post hoc Tukey HSD tests revealed that OW sig-
direction and distance from the outlet, had significant nificantly decreased with increasing sample depth.
main effects (F2,101 Z 122.36, F1,101 Z 179.77 and
F3,101 Z 5.00, respectively), at the 0.05 level, on periph- 3.1.2. Southern outlet
yton OW. The average OW to the north of the outlet Summer data indicated that sample depth and dis-
(1.908 G 0.149 g, 100 cmÿ2) was significantly higher tance from the outlet had a significant main effects
than to the south of the outlet (0.326 G 0.126 g, (F2,54 Z 3.907 and F2,54 Z 15.912, respectively), at the
100 cmÿ2). The greatest increase was observed at a depth 0.05 level, on periphyton OW. Tukey tests indicated OW
of 2 m, a moderate increase at 4 m and no increase at at 2000NE was significantly higher than reference site
8 m (Fig. 2B). Tukey tests revealed that OW measured OW at depths of 2 m and 4 m while a non-significant
from samples grown at 2 m depth and to the north of the increase was observed at 8 m (Fig. 3A). Post hoc Tukey
outlet were all significantly higher than the OW HSD tests indicated that average OW at 2 m and 4 m
measured from samples collected from the same depth were significantly lower than at 8 m.
 J. Cosgrove et al. / Estuarine, Coastal and Shelf Science 61 (2004) 331–338 335

1.0 3.2. Carbonate content

A. 2m
4m
0.8 8m Percentage carbonate content (%CO3) was useful
only in the calm conditions experienced in Whitfords
Lagoon during autumn (Fig. 4) and these will be the
0.6 only %CO3 results presented.

OUTLET
Sample depth and direction from the outlet had had
0.4 significant main effects (F2,101 Z 124.10 and F1,101 Z
38.34, respectively), at the 0.05 level, on periphyton
Organic Weight (g 100cm- 2 )

%CO3. Post hoc Tukey HSD tests found average

0.2
periphyton %CO3 at 4 m (7.962 G 0.643%) was slightly,
but significantly (P Z 0.040), higher than that observed
0.0 at 2 m (5.743 G 0.634%). Measurements of periphyton
1.0 %CO3 from samples at 8 m were substantially and
B. significantly higher (19.993 G 0.643%; P ! 0.001)
0.8
(Fig. 4).
At 2 m and 4 m depth periphyton %CO3 tended to be
lower at sites north of the outlet compared to the
0.6 reference site (Fig. 4). Tukey tests on 4 m data indicated
that periphyton %CO3 at 1000N and 2000N was sig-
0.4 nificantly lower than at the reference site. At 4 m depth
%CO3 was significantly positively correlated with
distance north of the outlet (r Z 0.560, P ! 0.010). At
0.2
a depth of 8 m there was a negative correlation between
%CO3 and distance north of outlet, mainly due to an
0.0 elevated reading (thought be a result of sedimentation)
2000NE 1000NE 500NE 4000S close to the outlet at 300N which was found by Tukey
*
Site tests to be significantly higher than all other values at the
0.05 significance level (Fig. 4).
Fig. 3. (A) Summer and (B) autumn periphyton organic weight
measured at sites of varying distance north and south of the Southern
outlet at 2 m, 4 m, and 8 m depth. Vertical error bars indicate standard
error. *Reference site. 4. Discussion

Wastewater significantly increased periphyton

Autumn data indicated that sample depth had a sig- growth. This effect was, however, limited in time and
nificant main effect (F2,59 Z 5.762) on periphyton OW, space presumably due to the influence of unmeasured
post hoc tests revealed that average OW at 4 m was
significantly lower than at 2 m and 8 m. 35

2m
30 4m
8m
Carbonate Content (%)

25
OUTLET

3.1.3. Laboratory experiment

Periphyton growth in aquaria produced substantially 20

less yield and appeared less diverse than growth in the

15
field.
One-way ANOVA results revealed a significant 10
difference in OW between treatments (F Z 12.485;
P Z 0.0073). Post hoc tests (Tukey HSD) revealed that 5
the control (unpolluted seawater) produced significantly
less organic weight than the treatments. The Northern 0
3500N 2000N 1000N 300N 300S 1000S 2000S
(primary wastewater treatment) and Southern (second- *
ary wastewater treatment) treatments were not signifi- Site
cantly different from each other (Fig. 5). Fig. 4. Variation of periphyton carbonate content measured at sites of
No significant variation of %CO3 due to treatment varying distance north and south of the Northern outlet during
was observed (data not shown). autumn. Vertical error bars indicate standard error. *Reference site.
336 J. Cosgrove et al. / Estuarine, Coastal and Shelf Science 61 (2004) 331–338

0.16 reference site was noted at 8 m depth. The lack of

0.14
a measurable effect on growth at a depth of 8 m may be
due to several factors, including reduced light availabil-
Organic weight (g 100cm-2)

0.12 ity, and a lesser degree of nutrient elevation (due to the

buoyant nature of the plume). Grazing may also be
0.10
greater closer to the benthos and hence may effectively
0.08 counteract a potential nutrient induced increase in
periphyton biomass as a result of wastewater discharge.
0.06
We propose that, due to the buoyant nature of the
0.04 plume, the shallower communities were more likely to
experience nutrient concentrations sufficiently elevated
0.02
to alleviate nutrient limitation, resulting in increased
0.00 biomass (OW). Observations indicated that ‘nuisance
Control Northern Southern species’ such Ulva rigida, Enteromorpha paradoxa,
(Unpolluted) (Secondary) (Primary)
Enteromorpha intestinalis, and Ectocarpus siliculosus
Treatment
provided most of the increased biomass in autumn.
Fig. 5. Variation in periphyton organic weight with treatment under These algal species favour high light and calm water
controlled conditions. Wastewater effluent was diluted 100-fold to (Arnold and Murray, 1980). Highest measures of
approximate minimum surface dilution in the field. Vertical error bars biomass at Sepia Depression sites were also recorded
indicate standard error.
during autumn. Lack of any impact of the wastewater
discharge at a depth of 8 m, in any season, suggests that
vertical mixing had provided sufficient dilution of the
factors impacting periphyton growth. While physical plume to return nutrient concentrations to background
variables such as light limitation, current speed and levels.
wind-related vertical mixing of the water column are During autumn around the southern outlet no such
likely to have acted to mitigate the impacts of nutrient influence of wastewater discharge on periphyton OW
enrichment around the wastewater outlets, grazing of was observed. There was a tendency for OW at a depth
periphyton may have acted to reduce the measured of 2 m to increase to the north-east of the outlet relative
influence of the wastewater discharge. Grazers have to the reference site OW, however, this trend was not
been found to increase grazing pressure in response to a significant one. Site 2000NE was shallower and closer
enhanced food availability and can effectively counter- to propagule sources (Fig. 1B) and the significant
act the positive influence of nutrient enrichment on (P ! 0.05) increase in OW at this site during summer
microalgal biomass (Hillebrand et al., 2000, 2002; (Fig. 3A) is thought to be a result of these factors rather
Hillebrand and Kahlert, 2001; Hillebrand, 2002). than any influence of the wastewater plume. Increased
Wind conditions were relatively calm during the proximity to propagule sources may also explain higher
autumn growth period. Data indicate that under these OW measured at 8 m compared to shallower treatments
conditions there is reduced wave-induced vertical mixing during both summer and autumn (Fig. 3A, B).
of the buoyant plume (Pattiaratchi et al., 1995) and Controlled growth experiments in aquaria utilising
therefore less dilution of the wastewater plume would 1% wastewater supported field observations (northern
have occurred than in summer. Physical disturbance (i.e. outlet), conducted in areas with greater than 1:100
sloughing) of periphyton would also have been at its wastewater dilution, that treated wastewaters enhance
minimum. In addition, decreased turbidity would have periphyton growth (Fig. 5).
led to improved light penetration and a decreased Values of periphyton percentage carbonate content
likelihood of light limitation, especially at greater (%CO3) were found to be somewhat variable due to
depths. These conditions probably reduced the influence suspended sediments settling on the artificial substrata,
of other limiting factors. Overall, the influence of treated especially at 8 m depth (often !2 m from the seabed).
wastewater (nutrients) became a more significant factor However, at Whitfords Lagoon %CO3 showed a signif-
for periphyton growth in autumn. icant positive correlation with distance north of the
During calm autumn conditions at Whitfords La- outlet in autumn at 4 m depth. At both 2 m and 4 m,
goon the buoyant treated wastewater from northern %CO3 of periphyton communities north of the outlet
WWTP would have rapidly risen to the surface and and in close proximity to the south were depressed
travelled predominantly in a northerly direction (Lord, compared to the reference site. Due to a lack of
2000). This resulted in enhanced periphyton growth exhaustive taxonomic studies it cannot be said whether
immediately north of the outlet at 2 m depth (Fig. 2B). this is due to nuisance species becoming more dominant
A similar but lesser effect was observed at 4 m (Fig. 2B). over slower growing encrusting coralline red algae and
No increase in periphyton growth relative to the other calcareous species, or simply the effects of
 J. Cosgrove et al. / Estuarine, Coastal and Shelf Science 61 (2004) 331–338 337

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measures appeared to be insignificant compared to that Hillebrand, H., Worm, B., Lotze, H.K., 2000. Marine microbenthic
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ties. Our findings in this study are supported by well-mixed coastal waters off Perth, Western Australia. Estuarine,
Thompson and Waite (2003), who found that phyto- Coastal and Shelf Science 39, 273–285.
Lewis, M., Boustany, R., Dantin, D., Quarles, R., Moore, J., Stanley,
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R., 2002a. Effects of a coastal golf complex on water quality,
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Acknowledgements coastal areas of the Gulf of Mexico. Archives of Environmental
Contamination and Toxicology 43, 11–18.
We wish to acknowledge the support from the Lord, D.A., 2000. Perth long-term ocean outlet monitoring pro-
Department of Commerce and Trade (Neville Stanley gramme. 1995–2000: Summary Report, Report No.95/022/8,
pp. 74. ISBN 1 74043 011 5, The Water Corporation, PO Box
bursary), University of Western Australia (Jennifer 100, Leederville WA 6902, Perth, Australia.
Arnold Memorial award) and Kinhill Engineering. JC Masseret, E., Amblard, C., Bourdier, G., 1998. Changes in the
also wishes to thank Des Lord and Associates for access structure and metabolic activities of periphytic communities in
to their documentation on the Perth Coastal Waters a stream receiving treated sewage from a waste stabilization pond.
Study, and the Water Authority of Western Australia Water Research 32 (8), 2299–2314.
Mattila, J., Räisänen, R., 1998. Periphyton growth as an indicator of
for access to Beenyup (northern) and Woodman Point eutrophication; an experimental approach. Hydrobiologia 377,
(southern) WWTP’s and for data on plume distribution. 15–23.
Neverauskas, V.P., 1987. Accumulation of periphyton biomass on
artificial substrates deployed near a sewage sludge outfall in South
Australia. Estuarine, Coastal and Shelf Science 25, 509–517.
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