Aquatic Botany, 24 (1986) 269--285 269

Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

THE LOSS OF SEAGRASS IN COCKBURN SOUND, WESTERN

AUSTRALIA. II. POSSIBLE CAUSES OF S E A G R A S S DECLINE

M.L. CAMBRIDGE 1, A.W. CHIFFINGS% C. B R I T T A N 3, L. MOORE ~ and A.J. McCOMB

Botany Department, University of Western Australia, Nedlands 6009 (Western Australia)
(Accepted for publication 25 February 1986)

ABSTRACT

Cambridge, M.L., Chiffings, A.W., Brittan, C., Moore, L. and McComb, A,J., 1986. The
loss of seagrass in Cockburn Sound, Western Australia. II. Possible causes o f seagrass
decline. Aquat. Bot., 24: 269--285.

This paper examines possible reasons for the extensive loss of seagrass in Cockburn
Sound following industrial development. Transplanted seedlings survived poorly in
Cockburn Sound compared with an adjoining embayment. Altered temperature, salinity,
sedimentation and water m o v e m e n t do n o t explain the death of seagrass over wide areas,
and there is no evidence for a role o f pathogens. Oil refinery effluent reduced seagrass
growth in aquaria at concentrations similar to those at the point o f discharge, but could
not account for the widespread deterioration observed in the field. Severe grazing by sea
urchins was observed on meadows already under stress and does not appear to be a
primary cause of decline; caged, transplanted seedlings also deteriorated.
Increased light attenuation by p h y t o p l a n k t o n blooms may have affected the depth to
which seagrasses could survive, but would have had little significant effect in shallow
water; marked p h y t o p la n k to n blooms were recorded only after extensive seagrass decline
had taken place. Light reduction by enhanced growth of epiphytes and loose-lying
blankets of filamentous algae in nutrient enriched waters is suggested as the most likely
cause of decline. Heavy epiphyte fouling was consistently observed on seagrasses in
deteriorating meadows, as well as on declining, transplanted seedlings, and is k n o w n to
significantly impair photosynthesis in other systems. Extensive seagrass decline coincided
with the discharge of effluents rich in plant nutrients.

INTRODUCTION

A marked reduction in the area of seagrass m e a d o w s has accompanied the

establishment of industry along the shores of Cockburn Sound, Western
Australia. The time-course of the reduction has been assessed in relation to

J Present address: Department of Marine Biology, University of Groningen, P.O. Box 14,
9750 AA, Haren, The Netherlands.
2 Also at Department of Conservation and Environment, 1 Mount Street, Perth, Western
Australia 6000.
3 Present address: Department o f Mines and Energy, Darwin, Northern Territory.

0304-3770/86/$03.50 © 1986 Elsevier Science Publishers B.V.

270

the establishment o f industry commencing in 1955: localized depletion t o o k

place by 1962, near to the p o i n t of discharge of effluent from an off re-
finery, and there were localized losses due to scouring near pylons, and to
physical processes such as dredging. However, widespread loss t o o k place
from 1969 onwards, and b y 1 9 7 8 a c c o u n t e d for 3300 ha, or some 97% of
the area originally occupied b y seagrass, representing a loss of some 83% of
organic p r o d u c t i o n b y these plants (Cambridge and McComb, 1984).
The work described here was concerned with assessing, for Cockburn
Sound, various factors which have been mentioned in the literature as
contributing to a decline of aquatic m a c r o p h y t e s in other regions; these
included altered temperature regimes, pathogens, effects of oil refinery
effluent, increased grazing pressure, change in water turbidity and increased
shading b y epiphytes. Attention was also directed to transplanting seagrasses
into the Sound from an adjoining, unpolluted e m b a y m e n t , so as to find o u t
whether the plants still survive poorly in the Sound.

MATERIALS AND METHODS

Transplant experiments

Seedlings were collected from Wambro Sound, an e m b a y m e n t 4 km south

of Cockburn S o u n d (Fig. 1), where Posidonia m e a d o w s are relatively un-
disturbed, and still grow d o w n to 11 m as t h e y once did in Cockburn Sound
(Cambridge and McComb, 1984).
An airlift was used to remove sediment from around the roots o f 2--3-yr
old seedlings of P. sinuosa Cambridge & Kuo. Comparable seedlings, each
2--3 leaves, were transferred to plastic tubes (8 cm diameter, 30 cm long).
F o r t y plants were returned to Warnbro Sound, and 40 to the experimental
site in Cockburn Sound. T w e n t y plants at each site were caged (0.5-cm mesh
sides, 1.0-cm mesh top) to prevent grazing. Leaf lengths were measured once
each week, and the cages brushed clean of marine growth either once or
twice each week.

Grazing

The extent o f sea urchin infestation was determined by underwater

surveys, and densities of animals associated with the various stages of sea-
grass denudation recorded from randomly-placed 1-m 2 quadrats at the
stations shown in Fig. 1.

Light, temperature, salinity and chlorophyll

These were measured every 2 months from August 1 9 7 8 to November

1979 at the sites shown in Fig. 1. Temperature and salinity were measured
with a temperature/salinity bridge {Hammond, Yeo-cal, Victoria).
 271

I
115"40' PermeliaBank Woodman
J ~ Point •

Sewage
,~0 • Outfall
• L
43: 32" 10'-

COCKBURN I

SOUND
e

BP
Oil Refinery
Outfall

Fertilizer Works
Outtall

Causeway with
Bridges

Rockingham

1 Shoa/water
Bay
B

A
#
÷
I

kilometres

WARN:RO
-32" 20' 32" 20'-
SOUND
Key
• Transplant sites
• Water sampling stations

115°4G ~ 115" 45'

I ~ I

Fig. 1. C o c k b u r n S o u n d a n d W a r n b r o S o u n d , W e s t e r n A u s t r a l i a , s h o w i n g sites f o r seagrass

t r a n s p l a n t s a n d c o l l e c t i o n o f w a t e r samples. N u m b e r e d circles are sites a t w h i c h sea-
u r c h i n d e n s i t i e s were m e a s u r e d . A t t e n u a t i o n c o e f f i c i e n t s o v e r seagrass m e a d o w s
( T a b l e I V ) w e r e m e a s u r e d a t sites A - - D .
272

Photosynthetically-active radiation was measured at 0.5-m intervals with a

q u a n t u m sensor (LiCor L a m b d a LI-185, Q u a n t u m Radiometer), and attenua-
tion coefficients calculated (Kirk, 1977).
F o r chlorophyll determinations, water (2 litres) was collected with a Nis-
kin bottle a metre below the surface, at mid-depth and a metre above the bot-
tom, passed through a glass-fibre paper (Whatman GFC), and chlorophyll a
was determined after 90% acetone extraction of the ground paper
(Strickland and Parsons, 1972).

Oil.refinery effluents

Seedlings of P. sinuosa and P. australis H o o k f. were collected from

Warnbro Sound as described for the transplant experiment. Four tubes were
placed in cylindrical glass aquaria (55 cm tall, 14 cm diameter) filled with
water from the collection site and maintained at 19 or 23°C in a constant-
temperature water bath under natural light in a glasshouse. Seedlings were
acclimatised for 14 days before a subsequent trial of 32 days; total leaf
growth was measured every 4 days. The water was aerated vigorously.
In the refinery, sea water passed through a separator (from which floating
oil residue was recovered), and the sea water, n o w containing off compo-
nents, discharged as an effluent on the shore of the Sound, at high-water
mark. Effluent was collected in darkened plastic drums from the point of
discharge into the Sound or, when higher concentrations were required, from
the separator. Concentrations o f effluent were expressed as hydrocarbons
using infra-red s p e c t r o p h o t o m e t r y (Perkin Elmer 283), calibrated using
h y d r o c a r b o n s from the separator (APHA, 1976).
Treatments of 0, 50 and 100% effluent were given to 6 replicates, with the
effluent--water m e d i u m changed every 8 days, giving an average m a x i m u m
h y d r o c a r b o n c o n t e n t of 1 ppm. In another trial, changing of effluelit--water
medium every 2 days tested the effects of an average hydrocarbon c o n t e n t
of 2 ppm. H y d r o c a r b o n concentrations were m o n i t o r e d during the course of
the trials, as aeration removed volatile c o m p o n e n t s .

RESULTS AND DISCUSSION

Seagrass transplants

Attention was concentrated on P. sinuosa, the main meadow-forming

species in the Sound. At the Warnbro station there was a marked gain in leaf
area, whereas the plants at the Cockburn Sound station showed a progressive
loss of leaf material (Figs. 2 and 3). N e w roots had grown on 90% o f the
plants at Warnbro, b u t there was no obvious r o o t growth at Cockburn
Sound.
There was a marked increase in a m o u n t of epiphytic algal growth at the
site in Cockburn S o u n d (Fig. 3). Before transplanting, the leaves supported a
 273

60-

50-

40-
g-
E

30-

20-

10-

Time (days)

Fig. 2. Change in leaf area of Posidonia sinuosa seedlings following transplanting from
Warnbro Sound to Cockburn Sound (circles) or to a control site in Warnbro Sound
(squares). Half of the plants at each site were covered with cages to exclude grazers
(broken lines), the other half were uncaged (solid lines). Vertical lines are standard errors.

f e w colonies o f e n c r u s t i n g c o r a l l i n e algae at t h e i r tips, a n d v e r y f e w fil-

a m e n t o u s algae. In W a r n b r o S o u n d t h e p l a n t s r e m a i n e d r e l a t i v e l y f r e e o f
t h e s e f i l a m e n t o u s e p i p h y t e s . H o w e v e r , in C o c k b u r n S o u n d , less t h a n 2 w e e k s
a f t e r t r a n s p l a n t i n g , t h e leaves w e r e c o v e r e d t o w i t h i n 2 c m o f t h e i r bases
w i t h h e a v y e p i p h y t i c g r o w t h s , especially at t h e s e n e s c e n t l e a f ends. T h e
m a i n g e n e r a w e r e Ectocarpus ( P h a e o p h y t a ) , Ulva a n d Enteromorpha
( C h l o r o p h y t a ) a n d Polysiphonia ( R h o d o p h y t a ) . L e a f surfaces o f all p l a n t s
were thickly coated by the third week. Strong wave action during a storm
t o r e a w a y m a n y o f t h e s e n e s c e n t l e a f e n d s a n d f i l a m e n t o u s algae, b u t a r a p i d
b u i l d - u p o f e p i p h y t e s o c c u r r e d again b e f o r e t e r m i n a t i o n o f t h e trial.
In s u m m a r y , t h e e n v i r o n m e n t o f C o c k b u r n S o u n d is clearly d e t r i m e n t a l t o
g r o w t h o f seagrasses, a n d t h e e f f e c t can b e o b s e r v e d w i t h i n a f e w w e e k s o f
t r a n s p l a n t i n g seedlings. P r e s u m a b l y t h e r e a s o n f o r this a d v e r s e e f f e c t is t h e
s a m e as t h a t w h i c h c a u s e d t h e d e c l i n e in seagrass m e a d o w s d u r i n g i n d u s t r i a l
development.

Temperature, pathogens and salinity

One possibility is t h a t t h e r e has b e e n a significant c h a n g e in t h e w a t e r

t e m p e r a t u r e o f t h e S o u n d , s u f f i c i e n t t o b r i n g a b o u t m e t a b o l i c stress or
p e r h a p s allow t h e invasion o f a p a t h o g e n {e.g. R a s m u s s e n , 1 9 7 7 ) . H o w e v e r ,
 274

Fig. 3. Transplanted Posidonia sinuosa seedlings after 48 days growth in either Warnbro
Sound or Cockburn Sound. Left, specimens photographed in air; the plant on the left is
from Warnbro Sound, that on the right from Cockburn Sound. Right, plants from
Cockburn Sound photographed underwater to show epiphyte growth.

w a t e r t e m p e r a t u r e s m e a s u r e d in t h e S o u n d d u r i n g t h e s t u d y w e r e c o m p a r -
able w i t h t h o s e in n e a r b y c o a s t a l w a t e r s , a n d w i t h l o n g - t e r m r e c o r d s a t
F r e m a n t l e ( H o d g k i n a n d Phillips, 1 9 6 9 ) .
T h e r a p i d i t y w i t h w h i c h t r a n s p l a n t e d seedlings d e t e r i o r a t e d in t h e S o u n d ,
t h e lack o f seagrass d i e b a c k in a d j a c e n t m a r i n e e m b a y m e n t s a n d t h e oc-
c u r r e n c e o f t h e s a m e species o f seagrass o v e r a w i d e l a t i t u d i n a l r a n g e
( M c C o m b e t al., 1 9 8 1 ) , also rule o u t t h e p o s s i b i l i t y t h a t a r e g i o n a l c h a n g e in
t e m p e r a t u r e m i g h t b e r e s p o n s i b l e f o r t h e d e c l i n e in C o c k b u r n S o u n d .
 275

It has been suggested that widespread mortality of Zostera marina L. is

due to invasion b y a microorganism (Rasmussen, 1977). In Cockburn Sound,
seagrass loss has been largely confined to the eastern shore, has n o t occurred
in adjoining e m b a y m e n t s and has involved several species. Examination of
plants from deteriorating m e a d o w s since 1970, and of transplanted seedlings,
has n o t disclosed evidence for pathogens such as leaf lesions.
The discharge of warm water m a y be detrimental to seagrass (Zieman and
Wood, 1975). In Cockburn Sound, release of warm-water effluent is very
localized on the eastern shore, showing an elevation of only 0.6°C at 1 m
depth, 100 m from the off-refinery outfall (December 1978). Any effect of
warm effluent on seagrasses w o u l d inevitably be confined to a small zone
around the p o i n t o f discharge.
Also, it would n o t be possible to explain the time course of seagrass
decline or t h e death o f transplanted seedlings b y a regional or local change in
salinity. Salinities measured in Cockburn Sound, Warnbro Sound and the
open ocean did n o t differ b y more than 1 % o .
Small quantities of groundwater flow into the nearshore shallows through
beach sands (Layton Groundwater Consultants, 1979), b u t Johannes (1980),
working some 50 km north of C o c k b u m Sound, f o u n d that groundwater is
rapidly diluted after entering the ocean. Although there are no data on the
effects of low-salinity interstitial waters in the substrate around the roots of
seagrasses, any effect would be very localized.

Altered sediment and water m o o e m e n t

Rapid sediment accretion m a y reduce the area of seagrass m e a d o w s

(Kirkman, 1978). However, in Cockburn Sound, the activities of man did
not greatly modify existing sedimentation patterns (France, 1978), except
locally, such as where scouring or dredging has occurred, and seagrasses were
locally eliminated (Cambridge and McComb, 1984).
Excessive water m o v e m e n t m a y alter the sediment regime, and m a y also
cause mechanical damage to plants. On the other hand, water m o v e m e n t is
important in the transfer of metabolites to and from submerged plants (e.g.
Sculthorpe, 1967). The construction of a solid-fill causeway (Fig. 1) has
reduced wave and current action across the Southern Flats, apart from areas
adjacent to the bridges where water is funnelled through relatively narrow
openings. P. sinuosa grows vigorously in the lee of the causeway where
annual primary production was the highest of all the stations measured
{Cambridge and McComb, 1984), b u t where the water is very calm except
under northerly wind conditions. In contrast, the entire eastern shore, where
major loss of seagrass occurred, is subject to strong wave action.

Grazing

Increased grazing, especially b y sea urchins, m a y be important in reducing

the areas of seagrass meadows. F o r example, heavy grazing b y sea urchins has
276

been reported from the United States in Thalassia testudinum Banks ex

KSnig (Camp et al., 1973) and Zostera marina meadows (Bak and Nojima,
1980). Ogden et al. (1973) recorded heavy grazing of seagrasses by a reef-
dwelling urchin in the West Indies. Urchins have been found to graze
Posidonia oceanica (L.) Delile in polluted areas of the Mediterranean, where
Posidonia was declining (Kirkman and Young, 1981) and in Botany Bay,
New South Wales, large populations of sea urchins have denuded Posidonia
meadows, following alterations in water movement due to harbour con-
struction (P. Anink, State Pollution Control Commission, New South Wales,
personal communication, 1983).
In Cockburn Sound, seagrasses are grazed by the sea urchin Temnopleuris
michaelsenii DSderlein, which is found in sheltered waters from South
Australia to Shark Bay (L. Marsh, Western Australian Museum, personal
communication, 1979). It is 1--3 cm in diameter, with sharp primary spines
3--4 mm long. Mortensen (1943) found only plant fragments, mainly sea-
grass, in the gut of this species collected from seagrass meadows. Grazed
leaves of Posidonia were found to have a jagged apex similar to that de-
scribed by Ogden et al. (1973) for seagrasses grazed by urchins in the West
Indies; this effect differed from the scalloped edges produced by fish grazing.
Marsh and Devaney (1978) report a survey of Cockburn Sound by the
Western Australian Naturalist Club in 1958--60, well before the onset of
seagrass loss, in which considerable numbers of this species of urchin were
found on the muds of the deep, central basin of the Sound, hut despite
extensive sampling, no large concentrations of the animals were found in the
seagrass meadows at that time.
T. michaelsenii was found to be locally abundant on occasions during the
present study. Table I shows densities recorded at stations along the eastern
shore of the Sound in November 1972. The highest density was in an area
carrying remnants of Posidonia meadows on the sand platform which was
once continuously vegetated by seagrass. Sampling stations in the more
severely-grazed meadow were divided into three categories: the centre of
exposed sand patches recently denuded of seagrass cover contained the
highest densities of. urchins (up to 250 m - : ) ; in seagrass at the edges of sand
patches where grazing was active, densities of urchins were found to be
intermediate (100 m - : ) ; and in the centre of the meadow or in patches of
seagrass between denuded areas leaves were less damaged and urchin den-
sities were lowest (up to 40--60 m - : ) . An underwater search made beyond
the sampled regions showed the most severely grazed area to be localised. At
the site of highest infestation, only a few animals could be found 6 weeks
later. However, the leafless plants did not recover, and on visits to the area
2 and 4 years later, no Posidonia was found. Thus, although high densities of
sea urchins appear to be short lived, their effects are more permanent.
Sea urchins invading in 1972 reduced much of the remnant meadow at
Rockingham (Fig. 1), isolated by the dieback of large areas of the eastern
shore meadows between 1969 and 1972, to bare sand. These were the most
 2,77

TABLE I

Densities of sea urchins at stations along the eastern shore of Cockburn Sound, November
1972

Station No. 1 Depth Number of sea urchins m - :

(m)
Seagrass meadow Denuded sand patches

Centre Edge of meadow

1 4 0,0 0,0 0
2 2 0,2 6,6,2 0
3 3 6,4 1,2 0
4 1--2 No seagrass No seagrass 0
5 2--5 8,4 3,3 6
6 4 40,60 100,106 206,250
7 4 8,11 10,12 11
8 2.5 No seagrass No seagrass 0
9 2--3 No seagrass No seagrass 0
10 1.5 0,0 0,0 0
11 1 0,0 0,0 0

1 Stations are given in Fig. 1. Duplicate quadrats were harvested at each site.

severe o u t b r e a k s o f u r c h i n grazing w h i c h we o b s e r v e d , b u t u r c h i n - d a m a g e d
Posidonia leaves a n d T. michaelsenii w e r e r e c o r d e d o n o t h e r o c c a s i o n s . F o r
e x a m p l e , in N o v e m b e r 1 9 7 2 small a r e a s o f seagrass w i t h g r a z e d a n d d a m a g e d
leaves w e r e o b s e r v e d a m o n g u n d a m a g e d seagrass o n a small s a n d - c o v e r e d r e e f
at Site 2 in Fig. 1, w i t h u r c h i n s p r e s e n t a t 2 0 G0 m - : a d j a c e n t t o a g r a z e d
p a t c h , a n d 0 - - 2 0 m - 2 in t h e m e a d o w . In D e c e m b e r 1 9 7 2 , Posidonia ad-
j a c e n t t o t h e s o u t h e r n bridge o f t h e G a r d e n I s l a n d c a u s e w a y h a d u r c h i n -
d a m a g e d leaves, a n d d e a d s e a - u r c h i n shells w e r e f o u n d a m o n g t h e sparse
r e m a i n i n g plants. In N o v e m b e r 1 9 7 3 , severe grazing was o b s e r v e d a t
C a r e e n i n g B a y ; t h e m e a d o w , w h i c h h a d originally e x t e n d e d d o w n a s a n d
slope t o 5 m , h a d r e c e d e d t o 2 m . A n o t h e r o u t b r e a k o c c u r r e d a t W o o d m a n
P o i n t in N o v e m b e r 1 9 7 6 .
O u t b r e a k s w e r e n o t c o n f i n e d t o C o c k b u r n S o u n d . A t a 1 0 - m - d e e p site in
W a r n b r o S o u n d , in F e b r u a r y 1 9 7 8 , sea u r c h i n s h a d r e m o v e d all leaves f o r
5 m u p s l o p e f r o m t h e original d e e p e r b o u n d a r y o f t h e m e a d o w . T h e a n i m a l s
w e r e p r e s e n t at a d e n s i t y o f a b o u t 2 0 0 m - 2 o n 3 F e b r u a r y a n d 6 M a r c h
1 9 7 8 , h a v i n g grazed a b o u t 0.5 k m a l o n g t h e edge o f t h e m e a d o w , as sur-
v e y e d b y u n d e r w a t e r t o w . N o a n i m a l s w e r e f o u n d 4 w e e k s later. G r e e n l e a f
m a t e r i a l was p r e s e n t b e n e a t h t h e s a n d o n 6 March, b u t b y 4 w e e k s later, f e w
living r h i z o m e apices c o u l d be f o u n d , a n d t h e r e w a s no r e g e n e r a t i o n in t h e
following year.
O n e f a c t o r was c o m m o n t o all o b s e r v e d i n s t a n c e s o f o v e r - g r a z i n g o f
Posidonia b y sea u r c h i n s ; t h e m e a d o w w a s a l r e a d y p a t c h y , d u e e i t h e r t o
278

deterioration of a once continuous m e a d o w , or to some natural environ-

mental limitation such as depth. There were no outbreaks in a well-
developed seagrass m e a d o w with a dense, continuous leaf canopy.
These observations, and the results o f the transplant experiment in which
caged plants deteriorated (Fig. 2), suggest that the large populations of sea
urchins which u n d o u b t e d l y denude areas o f deteriorating seagrass meadows,
are n o t the primary cause o f widespread loss o f seagrasses.

Effects of oil-refinery effluent

Seagrasses grew well during the period of the trials (8 weeks, including
2 weeks acclimatization), with growth rates which were comparable with
those observed in the field. Results of t w o of the trials are given in Table II,
where it can be seen that a significant reduction in leaf growth was ap-
parent when plants were subjected to an average concentration of 1 p p m
hydrocarbon. This concentration is comparable with that entering the Sound
at the high water mark, before extensive dilution u p o n mixing with the
waters of the Sound. There was no effect on P. australis under the same
conditions. Concentrations o f 10 ppm, at least 5 times that which enters the
Sound, were lethal to half o f the seedlings within a period of 2 weeks.
The low sensitivity of the plants to effluent is in contrast with the very
marked reductions in growth rates observed when seedlings were trans-
planted to the Sound (Fig. 3). The apparent short-term resistance of plants
to oil refinery effluent is consistent with the observations of Hatcher and
Larkum (1982), who found that leaf turnover of P. australis under con-
trolled conditions was n o t affected within 40 days at the highest concentra-
tion of oil which they used (363 g 1-1 ).
It is possible that chronic poisoning by effluent c o m p o n e n t s derived from
various sources, n o t just the oil refinery, m a y be important. Chegwidden
(1979) lists heavy metals, hydrocarbons and acids from effluents entering

T A B L E II

E f f e c t o f o i l - r e f i n e r y e f f l u e n t on the g r o w t h o f Posidonia australis u n d e r glasshouse

conditions

Temperature A p p r o x i m a t e h y d r o c a r b o n level ( p p m )
o f trial (° C)
0 0.5 1 2

19 25.0 (1.0) 22.5 ( 6 . 0 ) 19.0 ( 3 . 3 ) 2 --

23 28.3 ( 2 . 3 ) -- -- 16.8 (2.8) 3

~ R e s u l t s f r o m t w o trials are presented. Data are m e a n leaf g r o w t h , m m day - I , w i t h

standard e r r o r , f o r 6 seedlings.
D i f f e r e n c e f r o m c o n t r o l , P = 0.05---0.1.
3 D i f f e r e n t f r o m c o n t r o l , P < 0.01.
 279

the Sound. However, they were n o t d e t e c t e d in the waters of the Sound at

levels likely to be lethal over the time scale of the transplant trials.
It is also significant that despite the c o m m e n c e m e n t of release of effluent
from the oil refinery in 1955, it was 7 years before deterioration in seagrass
m e a d o w s could be seen in aerial photographs, as the loss of 4 ha of seagrass
in the region; this is in contrast with the major dieback of seagrasses which
occurred rapidly from 1969 onwards; approximately one year after the
c o m m e n c e m e n t of discharge from the fertilizer works (Cambridge and
McComb, 1984).
It is concluded that while the oil refinery effluent could have caused
localised death of seagrass near to the outfall, the extensive death of seagrass
along the eastern shore cannot be readily attributed to oil refinery effluent,
or to the discharge of inhibitory chemicals from other industries.

Light attenuation in the water column

Posidonia meadows once grew d o w n the slopes of the peripheral banks to

10--12 m, as indicated by the fibrous remains of rhizomes beneath the
sediment surface, b u t are n o w restricted to less than 3 m (Cambridge and
McComb, 1984). It is usually accepted that plants will colonise suitable
substrates to the depth where the light intensity allows photosynthesis to
exceed respiration on a yearly basis. Thus, any significant reduction in light
transmission through the water column will bring a b o u t a reduction in the
depth at which plants will survive. F o r example, Larkum (1976) has sug-
gested that increased turbidity has decreased the depth range of P. australis
in Botany Bay, New South Wales, w h e r e r e m n a n t s of seagrass m e a d o w s
extend only to 2.5 m, as compared with 7--9 m in the clearer waters of other
parts o f the New South Wales coast.
The mean light attenuation coefficient of water in Cockburn Sound was
generally twice that of the open ocean (Table III). Warnbro Sound was

TABLE III

Mean (S.E.) light attenuation and chlorophyll a concentrations for the plots shown in
Fig. 4

Attenuation coefficient

Ocean Warnbro Cockburn

0.07 (<0.01) 0.10 (0.01) 0.13(0.01)

Chlorophyll a (~g 1-1 )

Ocean Warnbro Cockburn

0.4 (< 0.1) 0.8 (0.2) 3.1 (0.3)

 280

similar to the open ocean in summer, but had higher attenuation coefficients
in winter (Fig. 4a), because of increased suspension of particulates by the
high wave energy o f winter storms and westerly swell.
Attenuation o f light in Cockburn Sound was usually considerably higher
than in Warnbro Sound; thus seagrasses at comparable depths would receive
less light in Cockburn than in Warnbro. Chlorophyll~ concentrations were
also considerably higher in Cockburn than in Warnbro Sound, where con-
centrations were generally similar to those of the open ocean (Table III,
Fig. 4b). The higher chlorophyll levels in Cockburn Sound are attributed to
the discharge of effluents rich in plant nutrients, of which nitrogen avail-
ability is critical (Chiffings, 1979; Chiffings and McComb, 1981).
Attenuation coefficients were generally greater over seagrass meadows in
Cockburn and Warnbro Sounds (Table IV) than the mean for the whole
water body (Table III). This may have been because of sediment resuspen-
sion, or materials released from the seagrass meadows.

0.18=

0.12-
0
(J
Z •'.,.• ••oO••••,"•,•
......... ." ;.,.,. ~...: ::.-:.."• " .. " •
0.06= °-.o•OO.*°*

J I Alsl°lNl°J d I F I M I A I MI JI a l A I s l o I " I OI
1977 1978
Months

8 •

O 2.
o
-r

° ,...... .~=_ ............... F .................... 1---4

, . , s,o
1977
I 1978
°I
Months

Fig. 4. Attenuation coefficient (above) and chlorophyll a content (below) for Cockburn
Sound (solid line), Warnbro Sound (dashed line) and a site in the open ocean (dotted
line). Sites are given in Fig. 1.
 281

S h a d i n g b y p h y t o p l a n k t o n b l o o m s , a n d b y l o c a l i z e d s u s p e n s i o n o f par-
t i c u l a t e m a t t e r , m a y well have b e e n i m p o r t a n t in t h e decline o f seagrasses in
d e e p e r w a t e r , w h e r e l i g h t was a l r e a d y at critical levels. O n t h e o t h e r h a n d , it
seems u n l i k e l y t h a t increased s e d i m e n t r e s u s p e n s i o n , or algal b l o o m s o f t h e
m a g n i t u d e o f t h o s e r e c o r d e d here, w o u l d have seriously i m p a i r e d light
availability t o m e a d o w s in shallow waters, d o w n t o a b o u t 5 m. In t h e trans-
p l a n t e x p e r i m e n t , t h e caged p l a n t s in W a r n b r o S o u n d received a p p r o x -
i m a t e l y t h e same light as t h e u n c a g e d plants in C o c k b u r n S o u n d ( T a b l e V),
y e t t h e p l a n t s in C o c k b u r n S o u n d grew at a m u c h l o w e r rate t h a n t h o s e in
W a r n b r o (Fig. 2).

TABLE IV

Attenuation coefficients at four seagrass stations in Cockburn and Warnbro Sounds,

1977--1979

Date Site ~ and Depth

Warnbro Sound Shoalwater Bay Cockburn Sound Cockburn Sound

A2.5m B3m C2.5m D1.0m

12 Dec. 1977 0.14 0.17 0.18 0.32

26 Jan. 1978 0.18 0.24 0.18 0.26
31 Mar. 1978 0.26 0.14 0.18 0.24
30 May 1978 0.40 0.25 0.39 0.94
1 Aug. 1978 0.22 0.17 0.30 0.20
29 Sept. 1978 0.08 0.12 0.11 0.21
16 Nov. 1978 0.09 0.13 0.10 0.14
Mean (S.E.) 0.19 (0.04) 0.17 (0.02) 0.21 (0.04) 0.33 (0.10)

Locations of Stations shown in Fig. 1.

TABLE V

Effect of water and cages on light penetration during seagrass trials 2

Locality Attenuation Light reaching seagrasses

coefficient
in water Above cages Within cages
(% of Warnbro cages)
(uE m - 2 s - 1 ) %
Cleaned Uncleaned

Warnbro Sound 0.13 (0.01) 2 965 100.0 74.5 69.8

Cockburn Sound 0.18 (0.02) 717 74.3 52.5 38.6

Data measured on 20 Nov., 23 Nov. and 14 Dec. 1978.

2 Standard error.
282

Deterioration of meadows occurred over the full depth range during the
period of major losses, and was not confined to a retreat of the deeper limit
of the meadow into shallower waters. Further, the onset of the major period
of seagrass dieback (1969) preceded the time (circa 1975) when phyto-
plankton blooms became prominent in the area. It is concluded that in-
creased light attenuation, brought about by phytoplankton blooms, was not
the primary cause of extensive loss of seagrass meadows.

The importance of epiphytes

Large quantities of epiphytes were consistently observed on seagrasses

where meadows were thinning, and growth of epiphytes was very marked in
the transplant trial (Fig. 3). On deteriorating meadows there were heavy
growths of red algae (including Acrochaetium, Laurencia, Centroceras and
Polysiphonia), green algae (including Enteromorpha and Ulva) and brown
algae (including Asperococcus). Individual plants were frequently large, up
to 25 cm long. These larger algae were much less common in Warnbro
Sound, and in Cockburn Sound where meadows were intact; in these areas
crustose coralline algae such as Melobesia were relatively more prominent. In
addition to true epiphytes, loose-lying blankets, up to 1 m thick, of fine
filamentous algae, predominantly Ectocarpus, were sometimes found over
remnants of seagrass meadows in Cockburn Sound.
As heavy epiphyte loads have been found to cause shading in seagrass
leaves sufficient to reduce photosynthesis and growth (Sand-Jensen, 1977;
Bulthuis, 1983; Bulthuis and Woelkerling, 1983; Orth and Montfrans, 1984),
it is suggested that the enhanced growth of epiphytes in nutrient-enriched
waters has brought about the decline in seagrass meadows in Cockburn Sound.
Nutrient levels are high in Cockburn Sound relative to nearby oceanic
waters, and favour phytoplankton growth (Chiffings and McComb, 1981).
Nitrogen is of particular importance in controlling phytoplankton growth in
the Sound {Chiffings and McComb, 1981) and, by implication, for the
growth of epiphytes as well.
Figure 5 shows the estimated levels of nitrogen entering the Sound from
industrial sources, with a summary of major events in the seagrass loss. A
marked increase in nitrogen loading coincided with the period of major
seagrass decline, providing circumstantial evidence for a link between in-
creasing nitrogen loads, enhanced epiphyte growth and deterioration of
seagrass. This suggestion is consistent with the findings of other studies,
which have reported increased growth of epiphytes and mats of filamentous
algae following nutrient enrichment (e.g. Moss, 1976; Phillips et al., 1978;
Harlin, 1980; Harlin and Thorne-Miller, 1981), and Fitzgerald ( 1 9 6 9 ) a n d
Shacklock et al., 1973 (cited Phillips et al., 1978) have emphasised the
importance of nitrogen availability.
 283
4000-

3000-
o
nitrogen fertilizer plant
2000-
t:
q
=_
1000- ll refinery . ~

19'60 1965 i 19J70 1~75 19'0o

Start of loss of major seagrass large

First records of
south of Kwinana (1969-70) phytoplankton blooms (1975-76)
Fig. 5. Estimated nitrogen loads entering Cockburn Sound (redrawn from A n o n , 1979),
showing the c o m m e n c e m e n t of discharge from the oil refinery, sewage t r e a t m e n t plant
and fertilizer works, together with the major time of seagrass loss (Cambridge and
McComb, 1984) and the first record of marked p h y t o p l a n k t o n blooms (Chiffings, 1979).

CONCLUSION

It is suggested that the following events have led to the major depletion of
seagrasses in Cockburn Sound:
(1) Increased nutrient loading, especially nitrogen, stimulated the growth of
epiphytes and unattached, filamentous algae.
(2) Increased algal growth significantly reduced the light available to seagrass
leaves. /
(3) Phytoplankton growth continued to increase water turbidity, further
reducing light intensity in areas distant from the points of nitrogen entry,
so that the deeper limit of these meadows retreated.
(4) As the canopy thinned, the seagrass meadow became vulnerable to
grazing by sea urchins. /

The third paper in this series more directly examines the hypothesis that
shading by epiphytes has been the primary cause of the loss of seagrass
meadows in the nutrient-enriched waters of Cockburn Sound (Silberstein et
al., 1986).

ACKNOWLEDGEMENTS

Financial support was provided by the Department of Conservation and

Environment, Western Australia. We are indebted to other members of the
Cockburn Sound Study Group for their help and advice, and to the Chem-
istry Department of the Western Australian Institute of Technology for the
use of the infra-red spectrophotometer.
284

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