P u b l i s h i n g

Marine
Freshwater
Research
Volume 53, 2002
CSIRO 2002

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in physical oceanography, marine chemistry,
marine and estuarine biology and limnology

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Marine and Freshwater Research
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Marine and Freshwater Research, 2002, 53, 11971210

Spatial and habitat-related patterns of temperate reef fish assemblages:

implications for the design of Marine Protected Areas
Belinda G. CurleyA,B,D, Michael J. KingsfordA,B and Bronwyn M. GillandersA,C
A

School of Biological Sciences AO8, University of Sydney, NSW 2000, Australia.

Current address: School of Marine Biology and Aquaculture, James Cook University, Qld 4811, Australia.
C
Current address: Department of Environmental Biology, University of Adelaide, SA 5005, Australia.
D
Corresponding author; email: belinda.curley@jcu.edu.au

Abstract. Patterns of rocky reef fish assemblages (composition and relative abundance of species) were examined
to provide data on the design of Marine Protected Areas (MPAs), which aim to protect these organisms. A
hierarchical design was used to investigate changes in fish assemblages at scales of metres to kilometres
along-shore, and among reef habitat types within two 10-km areas on the central coast of New South Wales,
Australia. Influences of physical and biological attributes of a reef on assemblages of fish were also examined. The
greatest variation in fish assemblages occurred at scales of 26 km along-shore. Eighty percent of species recorded
were found within a 6-km section of coastline. The most predictable differences in assemblages were found between
reef habitats (urchin-grazed barrens, Ecklonia forest and sponge habitat), and between depths. Marine Protected
Areas should ideally incorporate all available habitats over the entire depth range at which they occur. This may
require MPAs larger than 26 km, or multiple MPAs that have been specifically located to include these features,
as representation of habitats was found to vary at scales of kilometres to tens of kilometres along shore.
MF01 9
BeD.taiGlsg. nCoufrlMeyarineProtected Aeras

Introduction
Marine Protected Areas (MPAs) have been established
worldwide for the conservation of marine biota (Edgar and
Barrett 1999). The design of most MPAs, however, is driven
by economic and social factors, rather than the conservation
requirements of marine organisms (McNeill 1994). Marine
Protected Areas vary in size, shape and location, but there
has been little investigation of how such variables affect
conservation goals (Edgar and Barrett 1999). Although there
has been much discussion on the need for more rational
design of MPAs, and the ecological data required for such
design (e.g. McNeill 1994; Allison et al. 1998), few studies
have collected and interpreted data with MPAs specifically
in mind (but see McNeill and Fairweather 1993; Griffiths
and Wilke 2002).
The identification of relevant scales of natural variability
of marine organisms provides a valuable baseline for
ecologically relevant decisions on the design of MPAs, and
the evaluation of their success (Garca Charton et al. 2000).
These types of data are not available for most marine species,
particularly at small spatial scales. Although large spatial
patterns are useful in broad-scale zoning of MPAs such as
identifying bioregions, they do not provide the resolution
required for decisions on the design of MPAs at a local scale.
This is particularly true for highly urbanized regions, where
CSIRO 2002

the protection of tens of kilometres of coastline may not be

feasible because of conflicts among multiple users and the
impracticalities of enforcement.
The protection of reef fishes is often an objective of
MPAs. Reef fishes are conspicuous faunal components of
reef assemblages, and many species are harvested for food,
sport and bait (Kingsford et al. 1991). Changes in fish
assemblages affect other reef organisms, as many fishes
influence the dynamics of organisms through herbivory,
predation, feeding, excretion, and their role as prey
(Kingsford 1998). Studies of existing MPAs at different
latitudes and in different habitats have shown that the
abundance and mean size of exploited fish species are
generally greater within MPAs than in adjacent areas (e.g.
Babcock et al. 1999; Edgar and Barrett 1999).
Temperate reef fish assemblages vary at spatial scales
from metres to thousands of kilometres along-shore (Choat
and Ayling 1987; Kingsford 1989; Connell and Jones 1991;
Gillanders 1997). Most studies have focused on many
species at large biogeographical scales (Kingsford 2001), or
single species, trophic groups, and recently settled fishes at
smaller spatial scales (e.g. Lincoln Smith et al. 1991;
Holbrook et al. 1994; Gillanders 1997). Patterns of reef fish
assemblages at a range of small spatial scales (metres to tens
of kilometres) have not been quantified for most fish species.
10.1071/MF01199

1323-1650/02/081197

1198

B. G. Curley et al.

(c)

(a)

1
Terrigal
2

Pt Stephens
3

First Pt

Terrigal

4
5
N

Sydney

6
Third Pt
2 km

20 km

(d)
Magic Pt

(b)
2

Length of reefs in central NSW

Proportion in central NSW

0.4

Maximum
size of area

0.3

3
Botany Bay

0.2

0.1

9 10

Length of rocky reef (km)

Cape Solander
6
2 km

Fig. 1. (a) The central coast of New South Wales, Australia showing location of two study areas, Sydney and Terrigal.
(b) Frequency of lengths of naturally occurring units of rocky shores along the central coast of New South Wales (Port
Stephens to Port Hacking). (c) Terrigal study area (3329'S, 15127'E), and (d) Sydney study area (3359'S, 15115'E).
Shown are the locations (16) and the sites (within locations) in which fishes were sampled. The occurrence of habitat
types between 3 and 20 m depth varied as follows: Ecklonia forest, urchin-grazed barrens, and sponge habitat ();
Ecklonia forest and barrens (); barrens only (); turf habitat only ().

Temperate reef habitats (e.g. urchin-grazed barrens, kelp

forest) provide a diversity of resources for fishes, including
suitable prey, shelter and spawning sites (Schiel and Foster
1986; Buxton and Smale 1989; Tzioumis and Kingsford
1995). Spatio-temporal heterogeneity of reef habitats, and

the physical and biological attributes within a habitat (e.g.

depth, wave exposure, cover of macroalgae) have been
shown to be important in influencing the local distribution of
many fish taxa (Ebeling and Laur 1985; Choat and Ayling
1987; McCormick and Choat 1987; Kingsford et al. 1989;

Design of Marine Protected Areas

De Martini and Roberts 1990; Jones and Andrew 1990;

Lincoln Smith et al. 1991; Holbrook et al. 1994). Knowledge
of the relationships between habitat variability and fish
assemblages within biogeographical regions would provide a
more tangible framework for designing MPAs.
The main aim of this study was to provide data on
temperate reef fish assemblages (composition and relative
abundance of species) at spatial scales that are relevant to
decisions on the size and position of MPAs that seek to
protect these organisms. The specific aims were to: (i)
describe patterns of fish assemblages at scales of metres to
kilometres along-shore; (ii) describe patterns of fish
assemblages among habitats within reefs; and (iii)
investigate the degree to which variation in the physical
(depth and total width of reef) and biological (proportional
representation of habitats on a reef) attributes could account
for variation in assemblages of fish along-shore.

1199

estimate the relative area of each habitat and the total width of the reef
at seven sites. The distance at which habitats changed and the depth at
which these transitions occurred were recorded as a tape measure was
laid out perpendicular to the shore. Profiles ended at 100 m, 20 m depth,
or when the reef gave way to sand. Four profiles, approximately 20 m
apart, were completed at each site.
Temporal persistence of patterns
It is possible that patterns of fish assemblages at different spatial scales
or between different habitat types could have been confounded by
temporal changes between tides, hours, days, weeks, months and
seasons of sampling. Temporal variation was addressed in two ways.
The order in which sites and habitats within a site were sampled was
randomized. Sites separated by the largest spatial scales were,
therefore, not necessarily separated by the largest temporal scale. Also,
two habitat types at two sites within Sydney were sampled four times
during the 7-month sampling period. Both sites were sampled every 12
months on a random week, day, hour and tide. At each time, Ecklonia
forest and urchin-grazed barrens (within the same site) were sampled
on the same day.

Materials and methods

Study area and sampling of reef fishes
Spatial and habitat-related patterns of fish assemblages (composition
and relative abundance of species) were examined at multiple spatial
scales, using a partially hierarchical sampling design. Two 10-km areas
(Terrigal and Sydney) that were separated by approximately 50 km of
coastline were selected for sampling (Fig. 1a). Within each area, two
sites (separated by 300500 m) were selected at each of six locations
(separated by approx. 2 km) (Fig. 1c, d). These spatial scales reflected
naturally occurring units of reefs in this region. All reefs are less than
10 km in length, and 60% are less than 2 km (Fig. 1b). Sampling within
each site was stratified according to habitat type: urchin-grazed
barrens, Ecklonia radiata forest (hereafter Ecklonia forest), and sponge
habitat. Sites were sampled randomly and all data were collected
between March and September 1998.
Visual counts were used to sample fishes in replicate 25 5-m belt
transects as this transect size has been shown to give an acceptable level
of precision for a range of species, and generally fits into habitat units
found on reefs within New South Wales (Kingsford 1998). Counts were
made in six randomly placed transects within each habitat at each site.
Previously described physical and biological attributes of reef habitats
in New South Wales (Underwood et al. 1991) were used to distinguish
between habitat types. Cryptic and non-cryptic species were counted
using two different sampling techniques similar to those recommended
by Lincoln Smith (1989), to maximize the accuracy of estimates of
abundance. Non-cryptic species (e.g. Labridae, Monacanthidae,
Cheilodactylidae, Sparidae, Girellidae, some Pomacentridae,
Scorpididae and Plesiopidae) were counted 2.5 m either side of the
25-m tape measure as it was laid out. Cryptic species (e.g.
Pempherididae, territorial Pomacentridae and Serranidae) were counted
on the return trip along the same 25 5-m area by searching all
crevices, caves and other substrata. The abundance of schooling species
was estimated using log3 categories as recommended by Burchmore
et al. (1985) and Kingsford (1989). The median value of each category
was used in graphical representations and statistical tests. The same
person completed all counts, using SCUBA, between 0900 and 1600
hours when the water visibility was greater than 5 m.
Biological and physical attributes of habitats
Several attributes of reefs in Sydney were measured concurrent with
fish counts. The depth of each transect was recorded, and the mean
depth per six transects was used in analyses. Reef profiles were used to

Treatment of data
Multivariate and univariate techniques were used to examine spatial and
habitat-related patterns of fish assemblages. Because of the rarity of
sponge habitat (see Fig. 1), most analyses were only performed on data
collected in Ecklonia forest and urchin-grazed barrens. Data for
Terrigal were also not analysed because of a lack of multiple habitats at
most sites (see Fig. 1). Graphical representations of fish assemblages in
urchin-grazed barrens in Terrigal were used to further understand the
generality of patterns found at different spatial scales.
Multivariate techniques were used to examine variation in the
composition and relative abundance of species between habitats and at
different spatial and temporal scales, and between reef habitats with
different physical and biological attributes. A double square root
transformation was applied to all data to avoid dominance of common
species and to allow greater contributions from rare species (e.g. Clarke
and Green 1988). Species by sample matrices were converted to
similarity matrices using the BrayCurtis similarity coefficient.
Analyses of similarities included in the PRIMER computer program
(Clarke 1993) were used to test hypotheses concerning among-group
differences of composition and relative abundance of species.
Non-metric multidimensional scaling was used as the ordination
method (Clarke 1993). Stress values indicated how well the similarity
matrix was represented by the non-metric multidimensional scaling,
where stress tends towards zero when data are perfectly represented
(Clarke 1993). Between-group similarities (SIMPER) was used to
identify the major species contributing to dissimilarities among
habitats.
Speciesarea curves were constructed for Sydney and Terrigal to
determine how well species richness at small spatial scales (sites and
locations) are representative of species richness found at larger spatial
scales (between areas). Non-metric multidimensional scaling
ordination was used to incorporate the composition and relative
abundance of species into a cumulative speciesarea curve for the
Sydney area. The composition and relative abundance of species found
at Location 1 was compared with the composition and relative
abundance of species found at Locations 1 and 2 pooled and then both
were compared with Locations 1, 2 and 3 pooled and so on. All
locations were pooled to provide an estimate of the composition and
relative abundance of species for the entire 10-km length of coastline.
The error associated with speciesarea curves and the ordination plot
was investigated by repeating each process using a different starting
point (i.e. Location 1 to Location 6; Location 6 to Location 1).

1200

B. G. Curley et al.

Analysis of variance (ANOVA) was used to estimate variation in

abundance of numerically important fishes between urchin-grazed
barrens and Ecklonia forest at different spatial and temporal scales for
Sydney. Homogeneity of variances was tested prior to analyses using
Cochrans C-test (Winer et al. 1991). Variances were heterogeneous
(P < 0.05) for some species. Data for all species were therefore ln(x+1)
transformed so that the hypotheses tested were consistent for each
species. Analyses were performed if data remained heterogeneous
following transformation, as ANOVA is generally robust for
heterogeneous data (Underwood 1997). The factors location, site
(nested in location), and time were treated as random factors and habitat
type as a fixed factor in all analyses. Relationships between the physical
and biological attributes of reef habitats and abundances of numerically
important fishes were examined using correlation analyses.

Results
Habitat types

Percentage of species recorded

The along-shore distribution of reefs at Terrigal was patchy,

interrupted by several beaches 0.52 km in length. The width
of reefs sampled was generally less than 60 m (personal
observations). Reefs in Sydney are relatively continuous
along the 10-km study area, interrupted by two small
beaches approximately 0.5 km long, and the entrance to
Botany Bay. Reefs sampled ranged from 60 m to more than
100 m wide.
Three characteristic habitats were found and sampled
within the study areas: Ecklonia forest, urchin-grazed
barrens and sponge habitat. The occurrence of habitat types
varied between areas, locations and sites (Fig. 1c, d). Barrens
was the most frequently occurring habitat in both areas. This
habitat was found at nine of the 12 sites in Terrigal and all
sites in Sydney, at depths ranging from 3 to 20 m. Ecklonia
forest was found at two sites in Terrigal and all sites in
Sydney, at depths ranging from 3 to 10 m. Although Ecklonia
radiata was found at other sites in Terrigal, patches were less
than 125 m2. Sponge habitat was rare in both areas:

100
80

represented at one site in Terrigal and three adjacent sites in

Sydney. This habitat was recorded at depths of 1116 m.
A fourth habitat type, turf habitat, was found at three sites
at Terrigal, but was not sampled.
Patterns of composition and relative abundance of species
One hundred and eight species from 40 families were
recorded in the Sydney area. Seventy-seven species from 31
families were recorded in Terrigal, however, not all available
habitats were sampled at all sites. Sixty-four species were
recorded in both Sydney and Terrigal. Approximately 80%
of the total number of species recorded in urchin-grazed
barrens habitat (in Sydney and Terrigal) and all habitats
combined (Sydney only), were accounted for after the
inclusion of eight sites (approx. 6 km of coastline) (Fig. 2).
The composition and relative abundance of species was
similar at spatial scales of 4 km or more (Fig. 3a, b).
Urchin-grazed barrens generally contained a greater
number of species than Ecklonia forest (mean = 27.6,
s.d. = 6.4, n = 21; mean = 17.2, s.d. = 3.5, n = 13
respectively), and a similar number of species to sponge
habitat (mean = 30, s.d. = 2.6, n = 3). Non-metric
multidimensional scaling ordinations showed clear
differences in composition and abundance of species
between habitat types (Fig. 3c). Analyses of similarities
detected significant differences in composition and
abundance of species between urchin-grazed barrens and
Ecklonia forest only (R = 0.966, P < 0.001). Fifty percent of
the overall dissimilarity between habitats was accounted for
by 1318 species (Table 1). Principal contributions were
from species that were abundant in some habitats but
occurred in small abundances or were absent from others.
For example, Chromis hypsilepis and Pempheris compressa
were abundant in urchin-grazed barrens habitat only and
therefore were good discriminators for this habitat.
Pempheris multiradiata was a good discriminator for sponge
habitat. Small abundances of Trachinops taeniatus and
Hypoplectrodes maccullochi in Ecklonia forest would be
useful in discriminating between this habitat and
urchin-grazed barrens and sponge habitat.
Patterns of abundance for numerically important fishes

60

Barrens only, Terrig al

Barrens only, Sydney

40

All habitats, Sydney

20
0
0.5

10

Distance along shore (km)

Fig. 2. Speciesarea curves for urchin-grazed barrens habitat within

Sydney and Terrigal, and all habitats pooled in Sydney. Points along
each line show the sites at which samples were taken. Each curve
represents the mean of two curves that were calculated by using a
different start point (i.e. Site 1 to 12, and Site 12 to 1).

There was no evidence for a systematic increase or decrease

in abundances of fishes with distance along either study area.
The range of abundance of most species found in barrens
was similar for both study areas (Fig. 4). Parma unifasciata
(adults) and Parupeneus signatus were exceptions to these
results. Parma unifasciata decreased in abundance from
Location 1 (mean = 7 fish/125 m2) to Location 6 in Terrigal
(mean = 2 fish/125 m2), and occurred at only two sites in the
Sydney region (mean = 2 and 4 fish/125 m2). Parupeneus
signatus was more abundant in Sydney (maximum mean = 5
fish/125 m2) than in Terrigal (maximum mean = 1
fish/125 m2) (Fig. 4a).

Design of Marine Protected Areas

1201

(a)

stress=0.01
1
3
2

(b)

stress=0.00

2
3

5
(c)

stress=0.12

Fig. 3. (a, b) Non-metric multidimensional scaling ordinations

comparing the composition and relative abundance of fish species at
increasing spatial scales within Sydney. 1= The composition and
relative abundance of species within a 500-m section of coastline; 2 =
2 km; 3 = 4 km; 4 = 6 km; 5 = 8 km; and 6 = 10 km. (a) Ordination
when Location 1 was used as a starting point (see Fig. 1c.). (b)
Ordination when Location 6 was used as a starting point. (c)
Non-metric multidimensional scaling ordination comparing the
composition and relative abundance of species in urchin-grazed
barrens (), Ecklonia forest (), and sponge habitat () in Sydney
and Terrigal.

There were significant differences among locations for

one species, Opthalmolepis lineolatus (adults) (Fig. 4b;
Table 2). Similar numbers were, however, found for all
locations in the Terrigal area (Fig. 4b). Although densities of
juvenile labrids were low (Fig. 4c), mean values varied by a
factor of 24 among locations.
Nine species showed variation in abundance between sites
(within a location), and this was generally greater than
variation among locations. The former trend was consistent
for both Sydney and Terrigal (e.g. Fig. 4c, d). Significant
differences were detected between sites for the carnivores
Achoerodus viridis (adults), Pictilabrus laticlavius (adults),
and juvenile labrids, and for the planktivores C. hypsilepis
and T. taeniatus (Table 2). The herbivores/omnivores
Crinodus lophodon, Parma microlepis (adults and
juveniles), and Acanthaluteres vittiger and the planktivores
Atypichthys strigatus and Scorpis lineolatus also showed
differences among sites, but this difference depended on the
habitat examined (e.g. Fig. 4e; Table 2).
Differences in abundance were found between
urchin-grazed barrens and Ecklonia forest for 11 of the 16
species examined, including representatives from all trophic
groups (e.g. Fig. 4a, cf). Hypoplectrodes maccullochi,
P. signatus, C. hypsilepis, P. compressa, and T. taeniatus
were more abundant in barrens than in adjacent Ecklonia
forest (Table 2). Parma microlepis (adults and juveniles)
were also more abundant in barrens, but there was some
variation in the abundance of fish within each of these
habitats at different sites resulting in a significant interaction
between habitat and site in the analyses (e.g. Fig. 4e;
Table 2). Cheilodactylus fuscus (adults), and S. lineolatus
were generally more abundant in barrens habitat, however
this pattern was not consistent for all sites, particularly those
with a small abundance of fishes. Pictilabrus laticlavius
(adults), juvenile labrids, C. fuscus (juveniles), A. vittiger,
and Odax cyanomelas were significantly more abundant in
Ecklonia forests than in barrens (Table 2). The magnitude of
difference in abundance between habitats varied with site for
A. vittiger resulting in a significant interaction between
habitat and site in the analyses (Table 2). Crinodus lophodon
and A. strigatus also appeared to be more abundant in
Ecklonia forest, but this depended on the site examined.
Some taxa did not show clear differences in abundance
between habitats, including the carnivorous labrids A. viridis
(adults), Notolabrus gymnogenis (adults), and O. lineolatus
(adults). These species occurred in similar abundances in
both habitats at all locations (e.g. Fig. 4b).
The occurrence of sponge habitat within a site influenced
habitat-related patterns of abundance. The carnivores
H. maccullochi and O. lineolatus (adults) were more
abundant in sponge habitat than in adjacent Ecklonia forests
and urchin-grazed barrens (Fig. 5a, b). Cheilodactylus
fuscus (adults), P. signatus, P. microlepis (adults) and
T. taeniatus occurred in similar abundances in sponge

1202

B. G. Curley et al.

Table 1. Species contributing to greater than 2% of the dissimilarity between habitats: Ecklonia forest versus urchin-grazed
barrens (overall dissimilarity = 60.48%); Ecklonia forest versus sponge habitat (overall dissimilarity = 62.03%); urchin-grazed
barrens versus sponge habitat (overall dissimilarity = 51.08%)
Average abundance of fishes per site in each habitat in Sydney is given. Asterisks indicate the top three discriminating taxa for each habitat
Species
Chromis hypsilepis
Schuettea scalaripinnis
Atypichthys strigatus
Scorpis lineolatus
Pempheris multiradiata
Trachionops taeniatus
Hypoplectrodes maccullochi
Odax cyanomelas
Parupeneus signatus
Parma microlepis
Pempheris compressa
Apogon spp.
Upeneichthys lineatus
Optivus elongatus
Mecaenichthys immaculatus
Austrolabrus maculatus
Acanthaluteres vittiger
Pictilabrus laticlavius
Crinodus lophodon
Eupetrichthys angustipes
Dinolestes lewini

Average abundance
Ecklonia Barrens
Sponge
033.88
024.67
279.38
008.71
000.00
030.79
000.08
009.00
000.92
005.92
000.00
000.00
001.08
000.00
000.17
000.08
010.50
005.08
013.00
000.25
000.25

208.04
386.38
107.38
031.79
013.42
704.08
17.33
000.17
011.92
052.58
181.04
001.50
000.75
000.00
000.25
000.00
000.00
001.08
002.58
001.58
005.67

000.67
000.67
089.67
030.50
110.00
719.83
050.00
000.67
014.00
044.00
000.67
014.67
020.00
006.00
005.33
003.67
002.33
002.67
000.00
008.67
009.67

Ecklonia v. Barrens Ecklonia v. Sponge Barrens v. Sponge

%
%
%
5.29*
4.31*
3.30*
3.16*
2.27*
7.51*
4.01*
3.19*
2.84*
2.71*
6.99*

2.87*
2.09*

2.24*
2.00*
2.87*
2.57*
6.28*
7.61*
5.03*
2.56*
3.01*
2.37*

3.96*
3.18*
2.88*
2.72*
2.66*

3.31*
2.86*
2.14*

5.89*
3.72*
2.05*
3.39*
3.92*

5.47*
2.71*
3.14*
2.69*
2.23*
2.61*

habitat and in barrens, but were not as abundant in adjacent

Ecklonia forests (Fig. 5cf). The carnivorous labrids
A. viridis and N. gymnogenis occurred in similar abundances
in all three habitat types (Fig. 5 g, h). The remaining species
were not recorded in, or were in extremely small numbers, in
sponge habitat.

less than 10 m. No clear relationships between abundance

and depth were apparent for other taxa (e.g. A. viridis
(adults) and P. microlepis (adults); Fig. 6e, f). Relationships
between depth and abundance were not analysed for
Ecklonia forest as this habitat was generally found over a
very narrow depth range (37 m).

Biological and physical attributes of habitats

Temporal persistence of spatial and habitat-related patterns

The width of reefs in Sydney was variable. Five sites had an

average reef width between 58 and 88 m, and two sites
extended more than 100 m seaward. The proportion of each
habitat also varied markedly between sites. Urchin-grazed
barrens ranged between 32% and 49%, and Ecklonia forest
between 13% and 46%. Despite this variation, there was little
evidence to suggest that either attribute influenced fish
assemblages.
The depth of urchin-grazed barrens (320 m) was
correlated with the presence and abundance of some taxa.
Some species, such as Coris picta (comb fish) and
Paraplesiops bleekeri (eastern blue-devilfish), were
recorded only in urchin-grazed barrens that occurred at
depths greater than 13 m. Cheilodactylus fuscus (adults),
O. lineolatus (adults), and H. maccullochi were more
abundant with increasing depth (Fig. 6ac). In contrast,
P. microlepis (juveniles) (Fig. 6d) and P. signatus (r = 0. 581)
showed a negative relationship with depth and were
generally more abundant in barrens that occurred at depths

Spatial and habitat-related patterns of composition and

relative abundance of species were consistent among times
of sampling (Fig. 7a, b). The greatest variation in the
abundance of numerically important fishes occurred within
a sampling time rather than among different sampling times
and habitat-related patterns were persistent regardless of
time for most species. Relative abundance between sites was
dependent on the time of sampling for four species, A. viridis
(adults) (F = 4.553, P < 0.01), C. fuscus (adults F = 8.475,
P < 0.001, and juveniles F = 3.189, P < 0.05),
H. maccullochi (F = 0.326, P < 0.01), and A. strigatus
(F = 3.032, P < 0.05). Habitat-related patterns were not
consistent among sampling times for C. fuscus (juveniles,
F = 12.817, P < 0.001), but the mean number of fish
recorded was very small for both sites sampled (0.21.3).
Discussion
Fishes associated with temperate rocky reefs have a broad
range of biological characteristics that affect the way they

Design of Marine Protected Areas

1203

Sydney
7
6
5
4
3
2
1
0

Number of fish per 125 m2

Terrigal

(a) Parupeneus signatus

7
6
5
4
3
2
1
0

(b) Ophthalmolepis lineolatus (A)

(c) Juvenile labrids

(d) Trachinops taeniatus

280
210

140

140

70

70

(e) Parma microlepis (A)

(f) Hypoplectrodes maccullochi

* *

* *

* *

Fig. 4. Mean abundance (+ s.e.) of

numerically important fishes (adults (A),
juveniles or total numbers) in urchin-grazed
barrens () and Ecklonia forests (
\\ ) in
Sydney and Terrigal. Abundances are shown
for each of two sites (separated by
~ 300500 m) within each of six locations
(separated by ~ 2 km). *Site not sampled. n =
six replicates in each habitat at each site.
Juvenile labrids were <100 mm standard
length.

12

* *

397

210

350

280

12

* *

350

* *

Location
respond to their environment, and hence their distribution
and abundance through space and time. Despite this, it was
still possible to make generalizations that could provide a

practical and ecologically meaningful basis for the design

and monitoring of MPAs, which seek to protect these
organisms.

1204

B. G. Curley et al.

Table 2. Analysis of variance of the abundances of fishes in Sydney

The mean squares are shown for each species. Location and site were treated as random factors, and habitat as a fixed factor. Species
were analysed as total numbers, or adults (A) and juveniles (J). Cochrans C-test (C), and ANOVA were done on ln(x +1) transformed
data. *P < 0.05, **P < 0.01, ***P < 0.001. Cheilodactylus fuscus (J) were <150 mm standard length, juvenile labrids were <100 mm
standard length. L, Location; S, site; H, habitat; R, residual; d.f., degrees of freedom; s., significant.
Taxa
df =
error term =
Carnivores
Achoerodus viridis (A)
Notolabrus gymnogenis (A)
Opthalmolepis lineolatus (A)
Pictilabrus laticlavius (A)
Labrids (J)
Cheilodactylus fuscus (A)
Cheilodactylus fuscus (J)
Hypoplectrodes maccullochi
Parupeneus signatus
Herbivores/Omnivores
Crinodus lophodon
Parma microlepis (A)
Parma microlepis (J)
Acanthaluteres vittiger
Odax cyanomelas
Planktivores
Atypichthys strigatus
Chromis hypsilepis
Scorpis lineolatus
Pempheris compressa
Trachinops taeniatus

L
5
S(L)

S (L)
6
Res.

H
1
HL

HL
5
H S(L)

H S(L)
6
Res.

R
120

00.342
00.500
02.837*
00.212
00.510
00.390
00.099
00.751
01.058

00.650*
00.250
00.354
00.208*
00.704*
00.432
00.068
00.346
00.686

001.708
000.027
000.911
000.872*
006.482**
002.289*
000.494*
047.192***
012.165*

0.345
0.161
0.643
0.065
0.117
0.170
0.037
0.706
0.971

00.194
00.046
00.364
00.136
00.215
00.488*
00.039
00.358
00.254

0.227
0.171
0.237
0.070
0.273
0.223
0.067
0.164
0.333

s.
n.s.
n.s.
s.
n.s.
s.
n.s.
s.
s.

01.714
01.135
00.428
01.13
00.258

00.959*
00.578*
01.184***
01.056***
00.303

007.731
080.064***
026.387***
010.571*
017.36**

2.186
0.401
0.232
1.130
0.382

01.117***
00.611**
00.742**
01.056***
00.321

0.238
0.200
0.186
0.137
0.187

n.s.
n.s.
n.s.
s.
s.

11.956
12.278
02.464
01.99
02.651

10.909***
03.737*
02.148**
02.378
03.095*

000.145
145.277**
030.227**
147.982***
519.841***

4.528
3.712
0.767
1.99
3.459

14.484***
03.239
01.637*
02.378
01.407

1.777
1.497
0.672
1.238
1.051

s.
n.s.
s.
s.
s.

Along-shore patterns
The greatest variation in fish assemblages (composition and
relative abundance of species) occurred at small spatial
scales. Eighty percent of species found within a 10-km
section of coastline were accounted for in the first 6 km, and
the composition and relative abundance of species was
similar at spatial scales of 4 km or more. The greatest
variation in the abundances of most numerically important
fishes occurred at scales of metres to hundreds of metres,
rather than kilometres or tens of kilometres along-shore.
Although previous studies have demonstrated significant
differences in temperate reef fish assemblages at almost all
spatial scales (for reviews see Jones 1988; Kingsford 1998),
few have used a hierarchical approach to compare the
magnitude of variation among scales (but see Kingsford
1989; Syms 1995). This study is the first that we are aware
of that has been specifically designed to partition variance at
spatial scales relevant to the design of MPAs within a
biogeographical region.
The small-scale variation identified in this study has
several implications for MPAs that seek to protect reef
fishes. Because most variation in fish assemblages occurred
at scales between 2 and 6 km it is unlikely that few, randomly
placed MPAs that encompass smaller sections of coastline
will be representative of patterns found at larger spatial

scales within a biogeographical region. Furthermore,

although densities of recruits were generally small, densities
of some groups of fishes (e.g. juvenile labrids) varied by
factors of 24 at spatial scales of 5 km or more. Small-scale
variation (metres to kilometres) in the abundance of juvenile
fishes was also detected in a previous multiscale study
encompassing the same region (Lincoln Smith et al. 1991).
It is widely recognized that the relative importance of
ecological processes may depend on the size of fishes (Jones
1988). Different places along a coastline may be more
favourable for recruits, the supply of recruits may be variable
in time and space, or fishes in different places may have
variable patterns of growth (Kingsford 1998). These data
also suggest that small (<2 km), randomly placed MPAs are
unlikely to include suitable sites for recruitment of some
fishes.
Protection at relevant scales could be achieved by
protection of part of a continuous rocky shore, or a naturally
occurring unit of rocky shore such as a headland flanked by
sandy beaches. In central New South Wales, approximately
30% of naturally occurring units of rocky reefs are 26 km
in length (Fig. 1b). These units would provide clear
geological boundaries for MPAs. Linkages between habitats
should, however be carefully considered under this strategy,
as large areas of sand could prevent the post-settlement

Design of Marine Protected Areas

18

1205

(a) Hypoplectrodes maccullochi

(b) Opthalmolepis lineolatus (A)

6
12
4
6
2
0

Number of fish per 125 m 2

(c) Cheilodactylus fuscus (A)

14

(e) Parma microlepis (A)

350

12

(d) Parupeneus signatus

(f) Trachinops taeniatus

280

10
8

210

140

4
70

2
0
8

(g) Achoerodus viridis (A)

(h) Notolabrus gymnogenis (A)

Site
Fig. 5. Mean abundance ( s.e.) of fishes (adults (A) or total numbers) in Ecklonia forest (),
// urchin-grazed barrens
(), and sponge habitat () at three sites in Sydney. n = six replicates in each habitat at each site. Position of sites are given
in Fig. 1d.

1206

B. G. Curley et al.

(a) Cheilodactylus fuscus (A)

(b) Opthalmolepis lineolatus (A)

r = 0.716 **

0
0

Number of fish per 125 m2

r = 0.845 **

10

15

20

0
0

(c) Hypoplectrodes macullochi

15

20

r = 0.645 *

r = 0.722 **
6

10

15

20

0
0

10

15

20

(f) Achoerodus viridis (A)

(e) Parma microlepis (A)

16

r = 0.411

r = 0.345
12

0
0

10

(d) Parma microlepis (J)

0
0

10

15

20

0
0

10

15

20

Average depth (m)

Fig. 6. Relationship between mean abundance ( s.e.) of fishes (adults (A), juveniles (J), or total numbers) and depth in
urchin-grazed barrens at 12 sites in Sydney. n = six replicates at each site. Pearson correlation coefficient, r. *P < 0.05;
**P < 0.01.

Design of Marine Protected Areas

(a)

1207

stress=0.04

(b)

stress=0.05

B1
B1 B1
B1
B2
B2
B2
B2

1
K1
K1
K1 K1
K2
K2
K2
K2

1
1
1

2
2
2

Fig. 7. Non-metric multidimensional scaling ordinations comparing the composition and relative abundance of species
at two sites (1 and 2), at four random sampling times. (a) Comparison of urchin-grazed barrens (B) and Ecklonia forest (K).
(b) All habitats pooled.

movement of some fishes between habitats. For example,

linkages between estuaries and rocky reefs are important for
sustaining populations of the blue groper, A. viridis
(Gillanders 1997).
The scale at which the effects of MPAs are monitored is
also important (Garca Charton et al. 2000). For most of the
numerically important fishes described here, replicate
sampling will be required at scales of hundreds of metres if
comparisons among larger areas (MPAs v. unprotected areas)
are to be meaningful. Although the sampling method used in
this study was designed to improve estimates of abundance
of multiple species of fishes, accuracy and precision-related
compromises were invariably made. For example, estimates
of abundances of some planktivores were imprecise as they
were found in large numbers in some transects within a site,
but were absent in others. It should be noted, however, that
high variances among replicates are characteristic for
schooling fishes regardless of the methodology used
(Kingsford 1989). Alternative methods of sampling will be
required for some species if potential changes in numbers of
fishes as a result of protection are to be detected (see
discussion in Willis et al. 2000). For example, angling and
baited underwater video systems have been found to be
superior to Underwater Visual Census for estimating relative
densities of Snapper, Pagrus auratus inside and outside a
marine reserve in New Zealand (Willis et al. 2000).
It has also been suggested that the aggregation of
species-level data into functional and taxonomic groups may
be of value when establishing and monitoring MPAs (Garca
Charton et al. 2000). Although this approach would
undoubtedly be cost effective, our study suggests that
pooling data at the trophic level does not always provide
accurate representation of species-level patterns. For

example, of the seven carnivores studied, one exhibited great

variation in abundance at scales of kilometres, four at scales
of hundreds of metres, and two at scales of tens of metres. A
combination of biological characteristics of fishes, such as
abundance, schooling behaviour, associations with substrata
and mobility, may be more appropriate for pooling species
into groups for sampling (e.g. Lincoln Smith 1989).
Habitat-related patterns
The greatest and most predictable differences in fish
assemblages occurred between habitats (urchin-grazed
barrens, Ecklonia forest and sponge habitat). Most fishes
were exclusive to, or were more abundant within, a particular
habitat. The greatest dissimilarity in the composition and
relative abundance of species occurred between Ecklonia
forest, and those habitats in which Ecklonia was generally
absent (urchin-grazed barrens and sponge habitat).
Size-related differences in patterns of abundance between
habitats were found for some fishes. Large labrids were
found in similar abundances in barrens and Ecklonia forest,
but juveniles were more abundant in Ecklonia forest.
Size-related changes in patterns of abundance between
habitat types have been documented for labrids (Choat and
Ayling 1987; Gillanders and Kingsford 1998), and are
thought to reflect age-specific changes in diet (Gillanders
1995).
Habitat-related patterns are the rule rather than the
exception for temperate rocky reef fishes (e.g. Choat and
Ayling 1987; Holbrook et al. 1994), and provide perhaps the
most tangible framework for decisions on the size and
positioning of MPAs. Although the establishment of MPAs
may result in habitat change (e.g. urchin-grazed barrens
changing to algal-dominated habitats; Babcock et al. 1999;

1208

Shears and Babcock 2002), this has not been demonstrated

for all regions. In light of this lack of data, the protection of
the existing range of habitats would be the logical thing for
managers to do. This level of protection will optimize the
chances of protecting fish assemblages that are found, and
the available resources provided by rocky reefs within a
biogeographical region.
Encompassing multiple habitats in some areas may
require spatial scales greater than 2 km as the representation
of habitats varied at scales of kilometres to tens of kilometres
along-shore. Urchin-grazed barrens was the most common
habitat type occurring at most sites in both areas. In contrast,
Ecklonia forest was common in only one of the areas studied,
and sponge habitat was rarely found in either area at depths
less than 20 m. The types and representation of habitats in
this study are characteristic of the central coast of New South
Wales (see Underwood et al. 1991), and some species of fish
were found to be useful for discriminating between these
habitats. Large numbers of C. hypsilepis and P. compressa
were characteristic of urchin-grazed barrens, and large
numbers of P. multiradiata were good discriminators for
sponge habitat. Small abundances of T. taeniatus and
H. maccullochi were characteristic of Ecklonia forest. It
should be noted that different assemblages of fishes,
including Girellids, Chironemids and some Scorpididae, are
often found in the immediate subtidal and fringe habitat (<3
m) (Kingsford 2003), but were not sampled here.
Differences in the physical and biological nature of a
habitat type may explain some of the along-shore variation in
assemblages of reef fish. The depth at which a habitat occurs
can be an important variable in influencing patterns of
abundance of fishes among reefs and the nature of
relationships may depend on sex and maturity (McCormick
1989; Schroeder et al. 1994). Positive correlations between
abundance and depth of urchin-grazed barrens (320 m)
were found in this study for most of the carnivorous fishes
examined (e.g. O. lineolatus and C. fuscus). These fishes
were also more abundant in sponge habitat that occurs in
deeper water. Some species, such as the comb fish, Coris
picta and the eastern blue-devilfish, Paraplesiops bleekeri,
were recorded only in urchin-grazed barrens that occurred at
depths greater than 13 m. Juvenile fishes were more
abundant in shallow depths (e.g. P. microlepis; shallow
barrens habitat) or in habitats that occurred only in relatively
shallow depths (e.g. juvenile labrids; Ecklonia forest, 37 m;
see also Gillanders and Kingsford 1998). Therefore, MPAs
should ideally include habitats over the entire depth profile
at which they occur. Other known correlations for spatial
variability of fish assemblages that may be applied to MPA
management scenarios include wave exposure and
topographic complexity (Russ 1984; Jones 1988).
Habitat type and the depth at which habitat occurs should
also be considered when monitoring the abundances of
fishes following protection. Sampling should be stratified by

B. G. Curley et al.

habitat for most species so that more precise comparisons

between areas can be made. Cross-habitat sampling may be
used for the adult labrids A. viridis and N. gymnogenis, as
these species occurred in similar abundances in all habitats
sampled and appear to be more flexible in their use of
habitats. Juvenile labrids are more abundant in algal habitats
(Gillanders and Kingsford 1998).
Temporal variation
It could be argued that temporal variation in the fidelity of
fishes to reefs, variable recruitment success, and tidal,
diurnal and seasonal movement of species may confound the
spatial patterns described. Preliminary data indicated that,
although the composition and relative abundance of species
in some habitats did fluctuate over time, recognizable
patterns, by spatial scale and habitat were still persistent.
Furthermore, large changes in the abundance of common
species are required to alter patterns of rank abundance
(Holbrook et al. 1994) and changes in habitat fidelity have
not been demonstrated over long time periods (Holbrook
et al. 1994).
Abundances of numerically important fishes between
sites were dependent on the time of sampling for only four of
the 16 species examined. Although it is still possible that
temporal effects differed among sites, previous studies
suggest that although the abundances of fishes may change
over time, the relative differences among sites are preserved.
(e.g. Choat et al. 1988; Kingsford 1989; Gillanders and
Kingsford 1998). Long-term studies are urgently required to
further understand the stability of populations of temperate
reef fishes and how this may influence studies of spatial
patterns.
Conclusions
Our study demonstrates that a hierarchical sampling design
that encompasses multiple spatial scales and habitats can
provide data relevant to informed decisions on the design and
monitoring of MPAs. Other information such as data on
movement, larval dispersal/retention among local
populations, and variable recruitment may also be important
(e.g. McNeill 1994; Allison et al. 1998; Warner et al. 2000),
but should be specifically collected and interpreted to
address design criteria for MPAs. Our approach would
augment investigations within a larger framework.
Acknowledgments
Special thanks to M. Britt, R. Stevens, B. Stewart, S. Bush,
G. Stewart, A. Curley, D. Curley, G. Curley, K. Casey and G.
Ellem for their assistance in the field, and to T. Glasby for
valuable criticism of the manuscript. This work was
supported by the Fish Ecology Laboratory, University of
Sydney, and the Joyce W. Vickery Scientific Research Fund,
care of the Linnean Society of New South Wales. B.M.G.
was supported by an ARC Postdoctoral Fellowship.

Design of Marine Protected Areas

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