J Appl Phycol
DOI 10.1007/s10811-013-0158-5
Restoring seaweeds: does the declining fucoid Phyllospora comosa
support different biodiversity than other habitats?
E. M. Marzinelli & A. H. Campbell & A. Vergés &
M. A. Coleman & B. P. Kelaher & P. D. Steinberg
Received: 24 May 2013 / Revised and accepted: 17 September 2013
# Springer Science+Business Media Dordrecht 2013
Abstract Degradation and loss of natural habitats due to
human activities is a main cause of global biodiversity loss.
In temperate systems, seaweeds are a main habitat former
and support extremely diverse communities, including many
economically important species. Coastal urbanisation is,
however, causing significant declines of key habitat-forming
seaweeds. To develop successful management strategies such
as seaweed habitat restoration, it is necessary to first determine
E. M. Marzinelli and A. H. Campbell equally contributed to this article.
E. M. Marzinelli : A. H. Campbell : A. Vergés : P. D. Steinberg
Sydney Institute of Marine Science (SIMS), Chowder Bay Road,
Mosman, NSW 2088, Australia
E. M. Marzinelli : A. H. Campbell : A. Vergés : P. D. Steinberg
Centre for Marine Bio-Innovation and School of Biological, Earth
and Environmental Sciences, University of New South Wales,
Sydney, NSW 2052, Australia
E. M. Marzinelli : A. H. Campbell : A. Vergés
Evolution and Ecology Research Centre, School of Biological, Earth
and Environmental Sciences, University of New South Wales,
Sydney, NSW 2052, Australia
M. A. Coleman
Department of Primary Industries, NSW Fisheries, PO Box 4321,
Coffs Harbour, NSW 2450, Australia
B. P. Kelaher
Centre for Coastal Biogeochemistry Research, National Marine
Science Centre, Southern Cross University, Coffs Harbour,
NSW 2450, Australia
P. D. Steinberg
Advanced Environmental Biotechnology Centre, Nanyang Technical
University, Singapore 637551, Singapore
E. M. Marzinelli (*)
Centre for Marine Bio-innovation, University of New South Wales,
Bioscience, Bldg D26, Sydney, NSW 2052, Australia
e-mail: [email protected]
what additional ecosystem values are likely to be added
through restoration and to provide baseline data against which
goals can be established and success can be measured. The
habitat-forming fucoid Phyllospora comosa was once common on shallow subtidal reefs around Sydney, Australia’s
largest city, but disappeared in the 1980s, coincident with
heavy sewage outfall discharges. To provide the baseline data
necessary for restoring and managing Phyllospora in areas
from where it has disappeared, we quantified the community
composition and abundance of fish and large invertebrates
(abalone and sea urchins) in healthy Phyllospora habitats
and compared them to those in Ecklonia radiata (the other
major habitat-forming kelp in the region) as well as other
common shallow subtidal habitats. Fish assemblage structure
was similar between Phyllospora vs Ecklonia beds, but
Phyllospora supported much greater numbers of abalone
and urchins than any other habitat. This suggests that, in
terms of some components of the biodiversity it supports,
Phyllospora is functionally unique and not a redundant
species. Restoring this seaweed will, therefore, also contribute to biodiversity rehabilitation by restoring unique
faunal assemblages that are supported by Phyllospora ,
including economically important species.
Keywords Abalone . Biodiversity . Ecklonia radiata .
Functional redundancy . Kelp forests . Restoration
Introduction
Seaweeds are important “foundation” species in marine temperate systems (Bruno and Bertness 2001), providing habitat
structure, food and shelter to many organisms (Dayton 1985),
as well as playing a critical role in primary production and as
effective sinks of carbon (Mann 1973, 2000; Smith 1981;
Chung et al. 2011). Key species of seaweeds that provide
J Appl Phycol
crucial resources, sustain biodiversity and underpin other important ecosystem functions are, however, declining globally
mostly due to multiple human impacts such as urbanisation,
overfishing, nutrient loading and climate change (Connell
2007; Steneck et al. 2002; Airoldi and Beck 2007; Wernberg
et al. 2011). As a consequence, many systems have shifted
from complex and productive algal forests to simpler, less
productive and generally less desirable habitats, such as barrens or algal turfs, impacting significantly on the services
provided by these systems (see references above).
Despite some extensive conservation efforts, most degraded systems have not recovered, with between 50 and 90 % of
marine ecosystems remaining in an altered state (Lotze et al.
2011). This highlights the need for active intervention to
recover degraded systems and, consequently, habitat restoration is therefore becoming an increasing focus of interest
(Young et al. 2005). While attempted in many systems, restoration efforts often lack the critical ecological information
necessary for success and indeed the information necessary
to set sensible and achievable goals (Young et al. 2005;
Goodsell and Chapman 2009). Understanding the factors
responsible for the demise of seaweeds and the processes that
allow their re-establishment, as well as the biodiversity they
support, is essential for developing successful strategies for
the restoration and management of these important ecosystems (Connell et al. 2008), but this information is often
lacking. An equally important first step is to determine what
additional ecosystem values (e.g. greater diversity, higher
numbers of economically important species) are likely to be
added through the restoration of these habitat formers in order
to allow informed decisions on the desirability and/or benefits
of restoration and to provide the baseline data necessary to
establish the goals against which to measure restoration
success (Goodsell and Chapman 2009).
Phyllospora comosa (Labillardière) C. Agardh is a large
habitat-forming fucoid seaweed that forms extensive underwater forests on shallow rocky reefs throughout much
of temperate south-eastern Australia (Underwood et al.
1991). “Crayweed” (as P. comosa is known by local
recreational fishers) provides resources to a wide variety
of organisms, including economically important species of
fish, “crayfish” (spiny lobster) and abalone (Andrew 1999;
Bishop et al. 2010).
Phyllospora was once common and abundant on shallow
subtidal rocky reefs in Sydney, Australia’s largest city, until
the early 1980s, when it disappeared from the metropolitan
coastline (∼70 km), but persisted on reefs north and south of
this area (Coleman et al. 2008). Its disappearance from reefs in
Sydney coincided with a peak in high volume, near-shore
sewage outfall discharges along the metropolitan coastline
during the 1970s and 1980s (Coleman et al. 2008). Despite
significant improvements in water quality along the Sydney
coastline since the introduction of deep-water outfalls and the
decommissioning of near-shore outfalls in the early 1990s
(Scanes and Philip 1995; Sydney Water 2007), P. comosa
populations have not re-established in this area. The disappearance of this key habitat-forming seaweed is likely to have
had significant impacts on local biodiversity and function.
P. comosa is not the only habitat-forming seaweed in this
area. Forests of the kelp Ecklonia radiata (C. Agardh) J.
Agardh also characterise rocky coasts of south-eastern Australia (Underwood et al. 1991) and provide habitat for many
marine organisms (Kennelly and Underwood 1993; Goodsell
and Connell 2005). Despite co-occurrence over more than 10°
latitude, the extent to which the function provided by these
two species overlaps, in terms of the biodiversity they support,
is poorly understood.
Recent efforts to experimentally restore P. comosa habitat
in metropolitan Sydney have shown promising results, with
the successful establishment of small, reproductive and selfsustaining populations in reefs where this species was once
abundant (Campbell et al. in review). Prior to the establishment of a large-scale restoration program, however, it is necessary to quantitatively assess the biodiversity (i.e. numbers of
species, their identity and relative abundances) supported by P.
comosa relative to that supported by other habitat-forming
macroalgae, in order to provide baseline data for marine estate
management authorities and set sensible restoration goals.
In this paper, our aim was therefore to quantify components
of the biodiversity supported by the seaweed P. comosa ,
focusing on economically important abalone, sea urchins
and fish, and to determine whether these communities are
unique relative to the other major habitat-forming kelp
Ecklonia and other common shallow subtidal habitats.
Materials and methods
Sampling was done within the Batemans Marine Park
(35°42′ S 150°12′ E), NSW, Australia, where P. comosa is
still common and abundant on shallow subtidal rocky reefs, in
two separate sampling events.
In August 2011, abundances of abalone in P. comosa beds
were compared to those in E. radiata beds (the other dominant habitat-forming macroalga) and other typical shallow
subtidal habitats in NSW (Underwood et al. 1991). Sampling
was done in two randomly chosen sites separated by ca 10 km
that were characterised by the presence of P. comosa and the
other habitats. In the first site (Fullers: 36°15′49″ S, 150°08′
56″ E), abalone were counted in the following habitat types:
Phyllospora, Ecklonia, turf-forming algae and barrens (see
Underwood et al. 1991). In the second site (Dalmeny: 36°09′
56″ S 150°07′53″ E), neither Ecklonia nor turf-forming algae
occurred as distinct beds: Ecklonia individuals were sparse
and mixed with algal turfs, a habitat defined as “fringe”
(Underwood et al. 1991), so this habitat was also sampled.
J Appl Phycol
In both sites, the number of abalone in 3-min visual searches
(n =3–6) was quantified by snorkeling at 1–3 m depth. The
habitats surveyed in each site were at least 10 m apart and the
areas surveyed during each replicate search were separated by
at least 5 m.
In October 2012, we quantified abundances of abalone, sea
urchins and fish assemblage structure in Phyllospora and
Ecklonia habitats. To avoid potential confounding effects
due to movements of fish between neighbouring habitats, a
hierarchical sampling design was used where we randomly
sampled four sites dominated by either P. comosa (Corunna—
36°18′22″ S, 150°08′18″ E; Fullers—see above; Montague
North—36°14′33″ S, 150°13′35″ E; Golfcourse—36°12′
53″ S, 150°08′20″E) or E. radiata (South Fullers—36°17′
28″ S, 150°07′59″ E; Tollgate—35°45′02″ S, 150°15′23″E;
Yellow Rock: 35°43′33″ S, 150°07′53″ E; Montague lighthouse—36°15′05″ S, 150°13′23″ E). Sites were interspersed
to avoid spatial confounding and were at least 1 km apart.
Sampling was done at 3–5 m depth by SCUBA diving.
Abalone abundances were quantified by doing 3-min searches
(n =6) as described above. The relative abundances of roving
fish were counted on four replicate transects (25×5 m) per
site. Transects were separated by 10–20 m and the area
surveyed per site was ca 0.01 km2. Surveys were done swimming at a constant speed and counting and estimating the size
(total length) of all fish to the nearest 5 cm. Density estimates
were converted to biomass using allometric length–weight
regressions published in Froese and Pauly (2005). When there
was no information available for a particular species, allometric values were estimated using length–weight regressions for
species from the same genus (where possible) or family, as per
Froese and Pauly (2005). Small-sized cryptic species were not
counted. Sea urchins were quantified on the same transects on
the return swim, but along a width of 1 m (i.e. 25×1 m). All
surveys were done by the same four experienced divers to
reduce observer bias.
Analyses of variance were used to examine differences
among habitats for numbers of abalone, sea urchins, total
numbers of fish individuals, total fish biomass and fish species
richness (see tables for detailed explanation). Analyses were
done using GMAV 5 (Underwood and Chapman 1997). When
Cochran’s test for heterogeneity of variances was significant
and no transformation was appropriate, the analysis of variance was still done because it is robust to departures from the
assumptions (Underwood 1997). Where significant interaction terms were detected, Student–Newman–Keuls comparisons of means were used to determine which treatments
differed (Underwood 1997). Nonsignificant interactions with
p >0.25 were pooled (Winer et al. 1991).
Fish multivariate data (abundance and biomass) were
analysed using permutational multivariate analyses of variance (Anderson 2001) with the PERMANOVA add-on in
PRIMER v6 (Anderson et al. 2007). Similarity matrices based
on Bray–Curtis distances of square root-transformed relative
abundances and biomass or presence/absence data were generated for the analyses, which used 9,999 permutations of
residuals under a reduced model. To visualise multivariate
patterns in fish assemblages, non-metric multi-dimensional
scaling (nMDS) was used as an ordination method using
PRIMER v6 (Clarke and Gorley 2006).
Results
In 2011, Phyllospora beds supported much greater numbers
of blacklip abalone (Haliotis rubra) than adjacent Ecklonia
beds (between two and eight times higher), turf-forming algae
or fringe habitats (a mix of Ecklonia and algal turfs), which, in
turn, supported greater numbers of abalone than barrens
(Table 1, Fig. 1). In 2012, numbers of abalone in Phyllospora
were again significantly higher than the numbers found in
Ecklonia beds—more than 1 order of magnitude on average,
despite significant variability among sites within each habitat
type (Table 2, Fig. 2).
The total number of sea urchins was also significantly
greater in Phyllospora beds than in Ecklonia beds
(Table 3, Fig. 3a). Three species of urchins were recorded:
Centrostephanus rodgersii, which represented ca 93 % of the
total number of urchins quantified, Heliocidaris erythrogramma
and Phyllacanthus parvispinus, the latter being represented by
only two individuals (both in Ecklonia beds; Fig. 3a).
Overall, 602 fish individuals belonging to 22 species were
recorded. There were no significant differences in the total
number of fish, total fish biomass or the number of fish species
between Phyllospora and Ecklonia beds; rather, there was
significant variability among sites within each habitat (Table 3,
Table 1 Analysis of abalone abundance in Phyllospora vs Ecklonia,
turf-forming algae or barren (site 1) or “fringe” (i.e. Ecklonia + algal
turfs) or barren (site 2) in 2011
Site 1
Site 2
Source
df
MS
F
p
Ha
Residual
SNK
3
3.1
25.4
<0.01
8
0.1
Phyllospora > Ecklonia =
turfs > barren
df
MS
F
p
2
104.1 17.8 <0.01
15 5.8
Phyllospora > fringe =
barren
Habitat was fixed with four (site 1) or three (site 2) levels. The replicates
were the 3min time searches (site 1, n =3; site 2, n =6). Data in site 1 were
ln(X+1) transformed. Cochran’s test for heterogeneity of variances: site 1,
C =0.33 ns; site 2, C =0.49 ns
Italicised values are those statistically significant with significance level
alpha = 0.05 (i.e. those with p < 0.05)
Ha habitat, SNK Student–Newman–Keuls (comparisons of means were
used to determine which habitats differed), ns Non-significant
J Appl Phycol
Fig. 1 Mean (+SE) number of
abalone in 3-min searches in
Phyllospora vs other subtidal
habitats at two sites in 2011
(a n =3, b n =6)
Fig. 3b–d). Similarly, the structure (abundance and biomass)
and composition of fish assemblages varied significantly
among sites within habitats, but no significant differences
were found between habitats (Table 4, Fig. 4) despite some
observed separation between groups in the ordination (nMDS;
Fig. 4).
Discussion
We found that the declining seaweed Phyllospora supported
significantly higher numbers of abalone and urchins than the
other major habitat-forming seaweed in the region (SE Australia), the kelp Ecklonia, or other common habitats, although
there were no clear differences in fish assemblage structure in
Phyllospora vs Ecklonia beds. This suggests that, in terms of
the abalone and urchin species it supports (and particularly
regarding economically important species), Phyllospora is
not functionally redundant and once lost, cannot be replaced
by other large habitat-forming seaweeds. Restoring this seaweed in Sydney, from where it has disappeared (Coleman
et al. 2008), in an ecologically sensible way, could thus lead
to the restoration of a unique community that is not currently
supported by extant benthic habitats, including enhancing
abundances of economically important species that are important
to local industries.
The most striking difference between Phyllospora and the
other habitats surveyed was the abundance of abalone: 70–
80 % (2011) or 95 % (2012) of abalone found occurred within
Phyllospora beds, which supported on average ∼20 times
more abalone than Ecklonia . These results suggest a very
strong association between abalone and Phyllospora, which
could be due to the provision of food, habitat or both
(Shepherd 1973; Saunders et al. 2009). Although abalone feed
on seaweeds, their diet is mainly composed of red algae and
they largely avoid consuming brown algae (Shepherd 1973;
Fleming 1995). It seems, therefore, unlikely that abalone use
Phyllospora as a food source. Nevertheless, Phyllospora
could support a different understory assemblage of red algae
compared to Ecklonia, which could, in turn, influence abundances of abalone. Furthermore, Phyllospora (or understory
coralline algae) may facilitate settlement and/or metamorphosis
of abalone larvae, which often settle in response to chemical
Table 2 Analysis of abalone abundance in Phyllospora vs Ecklonia
habitats in 2012
Source
df
MS
F
p
Ha
Si(Ha)
Residual
1
6
40
38.5
4.3
0.5
9.0
9.2
0.02
<0.01
Habitat was fixed with two levels, site was random, nested in habitat, with
four levels. The replicates were the 3 min time searches (n =6). Data were
ln(X+1) transformed. Cochran’s test for heterogeneity of variances,
C =0.19 ns
Italicised values are those statistically significant with significance level
alpha = 0.05 (i.e. those with p < 0.05)
Ha habitat, Si site, ns Non-significant
Fig. 2 Mean (+SE; n =6) number of abalone in 3-min searches in
Phyllospora vs Ecklonia habitats at four sites in 2012
J Appl Phycol
Table 3 Analyses of total sea urchin abundance, fish abundance, fish species
richness and fish biomass in Phyllospora vs Ecklonia habitats in 2012
Source
df
MS
Ha
Si(Ha)
Residual
1
6
24
Urchin abundance
10,512 5.2
0.03
3,067
Pooled
1,743
Fish abundance
0.2
0
28.7
4.6
6.2
1
6
24
Fish richness
12.5
1.2
10.1
2.7
3.8
Fish biomass
1.2×109 1.0
1.1×109 Pooled
1.2×109
Ha
Si(Ha)
Residual
F
p
0.31
0.04
MS
F
p
0.94
<0.01
0.32
Habitat was fixed with two levels; site was random, nested in habitat, with
four levels. The replicates were the 25m transects (n =4). Non-significant
terms with p ≥0.25 were pooled. Data in fish richness were square root
transformed. Cochran’s test for heterogeneity of variances: urchin abundance, C =0.63, p <0.01; fish abundance, C =0.32 ns; fish richness,
C =0.38 ns; fish biomass C =0.99, p <0.01
Italicised values are those statistically significant with significance level
alpha = 0.05 (i.e. those with p <0.05)
Ha habitat, Si site, ns Non-significant
Fig. 3 Mean (+SE) a sea urchin
abundances (n =16), b total fish
abundance, c fish richness and
d total fish biomass (in grams) at
four sites (n =4) in 25 m transects
in Phyllospora vs Ecklonia
habitats in 2012
cues from specific algae (Roberts 2001) or their biofilms
(Huggett et al. 2005).
Alternatively, abalone may be more abundant in Phyllospora
beds because of the refuge they provide. Phyllospora beds often
seem to occur on exposed rocky reefs with greater structural
complexity than those where beds of Ecklonia occur (EM
Marzinelli, personal observation). Crevices and caves in the
rock can provide refuge from predation and abalone are often
confined to these spaces (Shepherd 1973). Thus, differences in
structural complexity of the substratum rather than the presence
of Phyllospora per se may cause the observed differences in
abalone among habitats. This could have implications for the
potential restoration of Phyllospora habitats into Sydney. For
instance, if abundances of abalone are influenced not only by the
presence of Phyllospora but also by the type of substratum
where it occurs (i.e. an interaction of both, having a synergistic
effect), then restoration outcomes would be maximised if seaweeds are restored in areas selected for the structure of the
substratum. Thus, before large-scale restoration of Phyllospora
into Sydney is attempted, experiments are needed to disentangle
direct and indirect effects of this seaweed from effects of the
type of substratum where this seaweed naturally occurs.
J Appl Phycol
Table 4 PERMANOVAs based on Bray–Curtis similarity measure for square root transformed relative abundances, presence/absence and square root
transformed biomass of fish in Phyllospora vs Ecklonia habitats in 2012
Abundance (square root)
Presence/absence
Biomass (square root)
Source
df
MS
pseudoF
p(perm)
MS
pseudoF
p(perm)
MS
pseudoF
p(perm)
Ha
Si(Ha)
Residual
1
6
24
7,411
4,428
1,782
1.67
2.48
0.09
<0.01
5,964
3,118
1,261
1.91
2.47
0.08
<0.01
8,968
5,505
2,856
1.63
1.93
0.12
<0.01
Habitat was fixed with two levels; site was random, nested in habitat, with four levels. The replicates were the 25 m transects (n =4). P values were
calculated using 9,999 permutations under a reduced model
Italicised values are those statistically significant with significance level alpha=0.05 (i.e. those with p <0.05)
Ha habitat, Si site, ns Non-significant
The abalone fisheries’ production in Australia (>4,500 t in
2011) has a combined yearly value of ∼$200 M and represent
15 % of the Australian total wild-catch production and 60 %
of the global wild-catch abalone production (see review
by Mayfield et al. (2012) and references therein). Most of
the production comes from Tasmania, Victoria and South
Australia; NSW is the smallest abalone fishery in Australia,
contributing ∼2 % of the national catch (Mayfield et al. 2012).
However, part of the reason for this has been the decline of
abalone stocks in NSW in the last 30–40 years due to natural
disturbances, disease (particularly in mid-NSW) and illegal
fishing (Mayfield et al. 2012). Ongoing state management
actions appear to be leading to a slow recovery of the fishery
(Mayfield et al. 2012). Given the strong association between
abalone and Phyllospora, restoring this declining seaweed
has the potential to accelerate the recovery of this valuable
fishery in the area. However, manipulative experiments
aimed at disentangling biotic effects of Phyllospora from
other abiotic effects that covary with the presence of this
seaweed (see above) are needed to provide sound information
for restoration.
Phyllospora habitats also supported significantly higher
numbers of sea urchins than Ecklonia habitats, particularly
of C. rodgersii . These findings are consistent with other
studies from southeastern Australia that show that C.
rodgersii can be abundant in patches of Phyllospora habitat,
while they are never present in high numbers in Ecklonia
habitats (Underwood et al. 1991). This association may again
Fig. 4 nMDS based on Bray–
Curtis similarity measure for a
square root-transformed relative
abundances, b presence/absence
or c square root-transformed
biomass of fish in Phyllospora
(grey triangles) vs Ecklonia
(white triangles) habitats
in 2012
be partly derived from greater structural complexity in the
Phyllospora habitat, as C. rodgersii is positively associated
with crevices (Andrew and Underwood 1989). In addition,
Phyllospora could also be more resistant to urchin grazing
than Ecklonia, but algal choice experiments done in Sydney
showed that there were no differences in amounts of algae
consumed by C. rodgersii between these and other common
algal species in the area, irrespectively of differences in their
phenolic content (Steinberg and van Altena 1992). The presence of high numbers of sea urchins may in turn be indirectly
influencing abalone abundance. In southeastern Australia,
adult abalone and C. rodgersii are often negatively associated,
probably as a result of competition for food (Shepherd 1973;
Andrew and Underwood 1992). However, urchins can have a
positive effect on juvenile abalone abundance via two mechanisms. On the one hand, sea urchins facilitate the growth of
crustose coralline algae (Andrew 1991), which induce abalone
settlement (Huggett et al. 2005). On the other hand, juvenile
abalone often shelter beneath sea urchins, which may thus be
protecting them from predators (Day and Branch 2002).
Indeed, many studies have shown a positive association between juvenile abalone and sea urchins throughout the world
(Rogers-Bennett and Pearse 2001; Mayfield and Branch 2000;
Tarr et al. 1996; Kojima 1981).
Fish community composition varied most strongly among
sites within each habitat, whereas we found no significant
differences between Phyllospora and Ecklonia beds. Temperate rocky reef fish assemblages generally display clear habitat-
J Appl Phycol
related patterns when comparisons are made between highly
distinct systems, e.g. between urchin barrens and seaweed
dominated habitats (Anderson and Millar 2004; Curley et al.
2002; Holbrook et al. 1994; Choat and Ayling 1987) or
between habitats differing in substratum type (e.g. limestone
vs granite reef; Harman et al. 2003). In contrast, our findings
suggest that the canopy-forming seaweeds used in our study
(Phyllospora and Ecklonia) provide a relatively similar habitat
for roving fish communities. We did not, however, quantify
small, cryptic fish species, which are likely to respond to smallscale differences in characteristics of the algal habitats. Therefore, there may be differences in these fish communities that
our study did not assess. Our interpretation of the results is thus
limited to the roving fish community and subsequent studies
should incorporate small, cryptic fish in the sampling designs
to determine fine-scale effects of these algal habitats.
Australia’s temperate reefs are dominated by seaweed forests that support unique and extremely diverse communities
that underpin valuable commercial and recreational fisheries
and ecosystem services with an estimated economic value of
$AUS17 billion (Poloczanska et al. 2007). Given the global
concerns about losses of key habitat-forming organisms such
as seaweed forests and the consequences these have on ecosystem properties and services, there is an urgent need for
sound information to successfully restore these degraded habitats and the diversity they support. This work is the first step
to providing the baseline data necessary to develop successful
restoration strategies to increase local primary productivity
and enhance habitat and food supply that underpin these
valuable ecosystems.
Acknowledgments This work was funded by a Discovery Grant
(DP1096464) from the Australian Research Council (awarded to PDS
and MAC), an Early Career Researcher grant to AV, EMM and AHC, an
Evolution and Ecology Research seed Grant to EMM, AHC and AV (both
from UNSW) and the Centre for Marine Bio-Innovation (CMB). This is
contribution # 112 from the Sydney Institute of Marine Sciences.
References
Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine
habitats of Europe. Oceanogr Mar Biol Annu Rev 45:345–405
Anderson MJ (2001) A new method for non-parametric multivariate
analysis of variance. Austral Ecol 26:32–46
Anderson MJ, Millar RB (2004) Spatial variation and effects of habitat on
temperate reef fish assemblages in northeastern New Zealand. J Exp
Mar Biol Ecol 305:191–221
Anderson MJ, Gorley RN, Clarke KR (2007) Permanova + for Primer:
guide to software and statistical methods. Primer-E, Plymouth
Andrew NL (1991) Changes in subtidal habitat following mass mortality
of sea-urchins in Botany Bay, New South Wales. Aust J Ecol 16:
353–362
Andrew NL (1999) Under southern seas: the ecology of Australia’s rocky
reefs. UNSW Press, Sydney
Andrew NL, Underwood AJ (1989) Patterns of abundance of the sea
urchin Centrostephanus rodgersii (Agassiz) on the central coast of
New South Wales, Australia
Andrew NL, Underwood AJ (1992) Associations and abundance of sea
urchins and abalone on shallow subtidal reefs in southern New
South Wales. Aust J Mar Freshwat Res 43:1547–1559
Bishop MJ, Coleman MA, Kelaher BP (2010) Cross-habitat impacts of
species decline: response of estuarine sediment communities to
changing detrital resources. Oecologia 163:517–525
Bruno JF, Bertness MD (2001) Habitat modification and facilitation
in benthic marine communities. In: Bertness MD, Gaines SD,
Hay ME (eds) Marine community ecology. Sinauer, Sunderland,
pp 201–220
Choat JH, Ayling AM (1987) The relationship between habitat structure and
fish faunas on New Zealand reefs. J Exp Mar Biol Ecol 110:257–284
Chung IK, Beardall J, Mehta S, Sahoo D, Stojkovic S (2011) Using
marine macrolagae for carbon sequestration: a critical appraisal. J
Appl Phycol 23:877–886
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial.
PRIMER-E, Plymouth
Coleman MA, Kelaher BP, Steinberg PD, Millar AJK (2008)
Absence of a large brown macroalga on urbanized rocky reefs
around Sydney, Australia, and evidence for historical decline. J
Phycol 44:897–901
Connell SD (2007) Water quality and the loss of coral reefs and kelp
forests: alternative states and the influence of fishing. In: Connell
SD, Gillanders BM (eds) Marine ecology. Oxford University Press,
Melbourne, pp 556–568
Connell SD, Russell BD, Turner DJ, Shepherd SA, Kildea T, Miller D,
Airoldi L, Cheshire A (2008) Recovering a lost baseline:
missing kelp forests from a metropolitan coast. Mar Ecol
Prog Ser 360:63–72
Curley BG, Kingsford MJ, Gillanders BM (2002) Spatial and habitatrelated patterns of temperate reef fish assemblages: implications
for the design of marine protected areas. Mar Freshwat Res 53:
1197–1210
Day E, Branch GM (2002) Effects of sea urchins (Parechinus angulosus)
on recruits and juveniles of abalone (Haliotis midae). Ecol Monogr
72:133–149
Dayton PK (1985) Ecology of kelp communities. Annu Rev Ecol Syst 16:
215–245
Fleming AE (1995) Growth, intake, feed conversion efficiency and
chemosensory preference of the Australian abalone Haliotis rubra.
Aquaculture 132:297–311
Froese R, Pauly D (2005) Fishbase. World Wide Web electronic
publication. http://www.fishbase.org
Goodsell PJ, Chapman MG (2009) Rehabilitation of habitat and the value
of artificial reefs. In: Wahl M (ed) Marine hard bottom communities:
patterns, dynamics, diversity, and change. Springer, New York,
pp 333–344
Goodsell PJ, Connell SD (2005) Historical configuration of habitat
influences the effects of disturbance on mobile invertebrates.
Mar Ecol Prog Ser 299:79–87
Harman N, Harvey ES, Kendrick GA (2003) Differences in fish assemblages from different reef habitats at Hamelin Bay, south-western
Australia. Mar Freshwat Res 54:177–184
Holbrook SJ, Kingsford MJ, Schmitt RJ, Stephens JS (1994) Spatial and
temporal patterns in assemblages of temperate reef fish. Am Zool
34:463–475
Huggett MJ, de Nys R, Williamson JE, Heasman M, Steinberg PD (2005)
Settlement of larval blacklip abalone, Haliotis rubra, in response to
green and red macroalgae. Mar Biol 147:1155–1163
Kennelly SJ, Underwood AJ (1993) Geographic consistencies of effects
of experimental physical disturbance on understorey species in
sublittoral kelp forests in central New South Wales. J Exp Mar Biol
Ecol 168:35–58
J Appl Phycol
Kojima H (1981) Mortality of young Japanese black abalone Haliotis
discus discus after transplantation. Bull Jap Soc Sci Fish 47:151–159
Lotze HK, Coll M, Magera AM, Ward-Paige C, Airoldi L (2011) Recovery of marine animal populations and ecosystems. Trends Ecol Evol
26:595–605
Mann KH (1973) Seaweeds: their productivity and strategy for growth.
Science 182:975–981
Mann KH (2000) Ecology of coastal waters. Blackwell, Malden
Mayfield S, Branch GM (2000) Interrelations among rock lobsters, sea
urchins, and juvenile abalone: implications for community management. Can J Fish Aquat Sci 57:2175–2185
Mayfield S, Mundy C, Gorfine H, Hart AM, Worthington D (2012) Fifty
years of sustained production from the Australian abalone fisheries.
Rev Fish Sci 20:220–250
Poloczanska ES, Babcock RC, Butler A, Hobday A, Hoegh-Guldberg O,
Kunz TJ, Matear R, Milton DA, Okey TA, Richardson AJ (2007)
Climate change and Australian marine life. In: Gibson RN, Atkinson
RJA, Gordon JDM (eds) Oceanography and marine biology, vol 45.
CRC Press, New York, pp 407–478
Roberts R (2001) A review of settlement cues for larval abalone (Haliotis
spp.). J Shellfish Res 20:571–586
Rogers-Bennett L, Pearse JS (2001) Indirect benefits of marine protected
areas for juvenile abalone. Conserv Biol 15:642–647
Saunders TM, Connell SD, Mayfield S (2009) Differences in abalone growth
and morphology between locations with high and low food availability:
morphologically fixed or plastic traits? Mar Biol 156:1255–1263
Scanes PR, Philip N (1995) Environmental impact of deepwater discharge
of sewage off Sydney, NSW, Australia. Mar Pollut Bull 31:343–346
Shepherd SA (1973) Studies on southern Australian abalone (genus
Haliotis).1. Ecology of 5 sympatric species. Aust J Mar Freshwat
Res 24:217–257
Smith SV (1981) Marine macrophytes as a global carbon sink. Science
211:838–840
Steinberg PD, van Altena I (1992) Tolerance of marine invertebrate
herbivores to brown algal phlorotannins in temperate Australasia.
Ecol Monogr 62:189–222. doi:10.2307/2937093
Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes
JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability,
resilience and future. Environ Conserv 29:436–459
Sydney Water (2007) Sydney’s deepwater ocean outfalls: long-term
environmental performance. Sydney Water, Sydney
Tarr RJQ, Williams PVG, Mackenzie AJ (1996) Abalone, sea urchins and
rock lobster: a possible ecological shift that may affect traditional
fisheries. S Afr J Mar Sci 17:319–323
Underwood AJ (1997) Experiments in ecology. Their logical design and
interpretation using analysis of variance. Cambridge University
Press, Cambridge
Underwood AJ, Chapman MG (1997) GMAV 5 for Windows. University
of Sydney, Sydney
Underwood AJ, Kingsford MJ, Andrew NL (1991) Patterns in shallow
subtidal marine assemblages along the coast of New South Wales.
Aust J Ecol 16:231–249
Wernberg T, Russell BD, Moore PJ, Ling SD, Smale DA, Campbell A,
Coleman MA, Steinberg PD, Kendrick GA, Connell SD (2011)
Impacts of climate change in a global hotspot for temperate
marine biodiversity and ocean warming. J Exp Mar Biol Ecol
400:7–16
Winer BJ, Brown DR, Michels KM (1991) Statistical principles in
experimental design. McGraw-Hill, New York
Young TP, Petersen DA, Clary JJ (2005) The ecology of restoration:
historical links, emerging issues and unexplored realms. Ecol Lett 8:
662–673