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Effect of grazing on coralline algae in seasonal, tropical, low-shore rock pools: Spatio-temporal variation in settlement and persistence

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Low-shore rock pools in Hong Kong are dominated by crustose coralline algae (CCA) all year round. Experiments manipulating grazer access to new surfaces and those with established CCA were used to investigate the spatial and temporal effects of grazers on establishment and persistence of CCA. During establishment, CCA were always the first macroalgae to recruit to new surfaces. Predictable algal colonization patterns were observed, although the extent and timing varied spatially (between pools) and temporally (with season and year). Grazing was the primary factor controlling the dominance of the CCA in low-shore rock pools, and seasonal differences in algal composition were only pronounced in the absence of grazers. On new surfaces, where grazers were excluded, the settling CCA were overgrown by competitively superior brown crustose algae (Ralfsia spp.) in summer and by non-crustose macroalgae (Ulva spp., Enteromorpha compressa, Hincksia mitchelliae and/or Colpomenia sinuosa) in winter. On CCA-colonized surfaces, E. compresa was, however, the dominant macroalga in winter in the absence of grazers. As a result of thermal stress in summer, the established CCA were commonly bleached, and new patches of bare surface were subsequently released. Such physical disturbance, hence, re-initiated colonization processes. The rapid re-colonization of CCA on new surfaces by lateral growth and new settlement suggests that CCA are resilient in nature, which results in them being the dominant macroalgae in the low-shore rock pools, all year round, in the presence of grazers.
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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 326: 99–113, 2006 Published November 17
INTRODUCTION
Disturbance has long been recognized as a primary
mechanism driving succession, in which loss of species
and biomass from marine habitats is followed by
subsequent settlement, recruitment, development and
growth of various species (Pickett & White 1985, Sousa
1985). In intertidal and subtidal habitats, hard sub-
strates are often covered by sessile invertebrates and
algae, and are frequently influenced by both abiotic
(e.g. physical heat stress) and biotic disturbances (e.g.
grazing by echinoids and molluscs; Moore 1972, Law-
rence 1975, Hawkins & Hartnoll 1983). Subsequent
consequences of such disturbances can be complex
processes in that they are often not predictable and are
dependent on different factors such as the extent, fre-
quency and type of disturbance at various spatial and
temporal scales (Farrell 1989, Airoldi 2000). Disturban-
ces that are intense enough to create patches of bare
surface (e.g. echinoid grazing, wave damage, summer
heat stress) are likely to have different subsequent
events and consequences than those that are subtle,
non-lethal, or only cause partial or selective removal of
biomass (e.g. molluscan grazing; Steneck et al. 1991,
Dethier & Steneck 2001). Paths of succession are also
affected by the type and characteristics of the new
space colonizers, for example, the availability or rate
of arrival of new recruits (i.e. larvae and algal pro-
© Inter-Research 2006 · www.int-res.com*Email: hrsbwga@hkucc.hku.hk
Effect of grazing on coralline algae in seasonal,
tropical, low-shore rock pools: spatio-temporal
variation in settlement and persistence
Tak-Cheung Wai, Gray A. Williams*
The Swire Institute of Marine Science, Department of Ecology and Biodiversity, The University of Hong Kong,
Pokfulam Road, Hong Kong, SAR, China
ABSTRACT: Low-shore rock pools in Hong Kong are dominated by crustose coralline algae (CCA) all
year round. Experiments manipulating grazer access to new surfaces and those with established
CCA were used to investigate the spatial and temporal effects of grazers on establishment and
persistence of CCA. During establishment, CCA were always the first macroalgae to recruit to new
surfaces. Predictable algal colonization patterns were observed, although the extent and timing
varied spatially (between pools) and temporally (with season and year). Grazing was the primary
factor controlling the dominance of the CCA in low-shore rock pools, and seasonal differences in
algal composition were only pronounced in the absence of grazers. On new surfaces, where grazers
were excluded, the settling CCA were overgrown by competitively superior brown crustose algae
(Ralfsia spp.) in summer and by non-crustose macroalgae (Ulva spp., Enteromorpha compressa,
Hincksia mitchelliae and/or Colpomenia sinuosa) in winter. On CCA-colonized surfaces, E. compresa
was, however, the dominant macroalga in winter in the absence of grazers. As a result of thermal
stress in summer, the established CCA were commonly bleached, and new patches of bare surface
were subsequently released. Such physical disturbance, hence, re-initiated colonization processes.
The rapid re-colonization of CCA on new surfaces by lateral growth and new settlement suggests
that CCA are resilient in nature, which results in them being the dominant macroalgae in the low-
shore rock pools, all year round, in the presence of grazers.
KEY WORDS: Crustose coralline algae · Herbivory · Settlement · Summer heat stress · Persistence ·
Spatial and temporal variation
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 326: 99–113, 2006
pagules) and their ability to compete and reproduce in
the new environment (Connell & Slatyer 1977, Sousa
1984).
In intertidal and subtidal habitats, crustose coralline
algae (CCA; Corallinales: Rhodophyta) are widely dis-
tributed and occupy much of the primary substrate
(Johansen 1981). After disturbance, CCA are often the
primary colonists of hard substrates in these habitats,
and their subsequent survival (i.e. persistence) and
dominance (e.g. coralline barren grounds) are associ-
ated with intense grazing activity in many shallow
marine habitats (Lawrence 1975, Steneck 1986). The
processes of establishment of CCA and the succes-
sional pathways of algal groups on coralline-domina-
ted substrates under different grazing conditions at
various spatial and temporal scales are, however, not
well understood in many marine habitats (but see
McClanahan 1997, Coleman 2003).
In low-shore rock pools in Hong Kong, CCA are
the dominant algal group all year round (Hall-
Spencer 1994). Although grazing is known to be an
important factor in algal settlement in these pools
(Williams et al. 1995), spatial (e.g. between pool) or
temporal (e.g. between season) variation in primary
algal settlement and persistence (i.e. the continued
existence/survival) of established CCA has not been
investigated. The persistence of coralline algae is un-
likely to be solely affected by herbivore-induced dis-
turbance; as other factors, such as seasonality, water
motion, etc., are also likely to be important (see
Johansen 1981, Airoldi & Virgilio 1998, Connell 2003).
In addition, the corallines themselves influence persis-
tence, as they may either facilitate or inhibit the set-
tlement and growth of epiphytes, including erect
macroalgae (see Bulleri et al. 2002). The ecological
processes and mechanisms responsible for the per-
sistence and succession of coralline algae are, there-
fore, complex, and may vary in different environments.
Seasonal factors are known to be especially impor-
tant for coastal systems in Hong Kong,
since the hot, wet summer and cold,
dry winter have a strong influence on
the distribution and diversity of sessile
assemblages, especially macroalgae
(Hodgkiss 1984, Williams 1993, Kaeh-
ler & Williams 1996, Kennish et al.
1996). Successional processes can ope-
rate on different temporal scales (e.g.
season) and profoundly influence the
organization of assemblages (Bene-
detti-Cecchi 2000), especially in a
strongly seasonal environment such as
Hong Kong. The present study investi-
gates the effect of spatial (between
pools) and temporal variation (be-
tween seasons and years) in grazing, as a form of dis-
turbance, on primary settlement and persistence of
CCA, to determine whether there are any predictable
patterns of algal succession and development in low-
shore pools on seasonal, tropical shores.
MATERIALS AND METHODS
Site description and study period. A number of low-
shore rock pools (Pools 1, 4, 5, 6, 8 and 9; all 1.5 m
above Chart Datum, C.D.; Table 1) inside the Cape
d’Aguilar Marine Reserve, Hong Kong (22° 12’ N,
114° 15’ W) were randomly chosen (see Morton & Har-
per 1995 for detailed shore description). As Hong Kong
experiences a strongly seasonal climate, dominated by
2 monsoons, experiments were conducted during both
summer (June to October, monthly air temperatures
25 to 29°C, maximum 36°C, water temperatures ~27°C
and >80% of annual rainfall —designated the hot, wet
season) and winter (November to March, monthly air
temperatures 15 to 18°C, water temperatures ca.
17°C —designated the cold, dry season; see Kaehler &
Williams 1996 for climatic details).
In all rock pools, CCA were the most abundant algal
group and dominated the pool substrates (>70% cover)
all year round. The most abundant molluscan grazers
were Chlorostoma argyrostoma, Lunella coronata and
Nerita albicilla. Small numbers of limpets Cellana
toreuma and the sea urchin Anthocidaris crassispina
were also present (see Wai 2004, Wai & Williams 2006
for more details).
Primary algal settlement. Experimental design:
Poly-vinyl chlorinated (PVC) plates were used to pro-
vide a uniform and repeatable sampling unit (Smith et
al. 2001). New bare PVC plates (grey, 25 ×16 ×0.4 cm)
were roughened on a belt sander (Sandpaper Grade
180 for 1 min) and fixed using plastic bolts embedded
into a series of holes drilled ~5 cm below the pool sur-
100
Pool Max. Max. Volume Tidal Mean Max.
length ×width depth (l) level daytime daytime
(cm) (cm) (cm + C.D.) low tide low tide
(h; SD) (h)
1 622 ×220 102 4230 105 3.71 (2.05) 6
4 728 ×124 149 3843 150 7.19 (2.66) 12
5 468 ×172 145 3537 150 7.19 (2.66) 12
6 688 ×236 168 8266 150 7.19 (2.66) 12
8 466 ×96 65 881 150 7.19 (2.66) 12
9 1412 ×746 124 39 581 150 7.19 (2.66) 12
Table 1. Summary of physical characteristics, tidal level and mean daytime
(07:00 to 18:00 h) isolation period in relation to local predicted tidal patterns
(August 2000, Waglan Island, Hong Kong Observatory) of the experimental rock
pools at Cape d’Aguilar, Hong Kong (C.D.: Chart Datum)
Wai & Williams: Effect of grazing on coralline algae
face using epoxy putty (wet surface epoxy putty, Dev-
con). The bolts allowed the PVC plates and associated
treatments to be easily removed for repeated sampling.
Plates were assigned to 3 treatments: (1) cage, (2)
fence and (3) open. The cage treatment was made of
galvanized wire mesh (mesh size 1.5 cm, 30 ×20 ×
8 cm) and excluded macrograzers (>1.5 cm) from the
plates. The fence treatment was used as a cage control,
made in the same way as cages but without the two
20 ×8 cm sides, so the open sides allowed grazers ac-
cess to the plates. The open treatment was a control,
with plates only and free access for grazers. Four repli-
cates were randomly established for each treatment, in
each of 3 pools (Pools 1, 4 and 6; n = 3 pools ×3 treat-
ments ×4 replicates = 36).
Sampling protocol and data analysis: Experiments
were repeated in 2 different years in summer (May to
October, 2000 and 2001) and winter (November to
March, 2000-01 and 2001-02). The experiments ran for
4 mo in each season, and, every month, plates were re-
moved from the pools during low tide and transferred
(inside a cool box with seawater) to the laboratory (~10
to 20 min walk) for measurements, and then returned to
the same position during the next low tide (i.e. within
12 to 24 h). Two scales of photo-quadrats were taken of
each plate: (1) macro-quadrats (15 ×10 cm; n = 1), to
record any sea urchin graze marks, and (2) randomly
located ‘micro’-quadrats (1.5 ×1 cm; n = 12), to record
percentage cover of target groups using a binocular
microscope (magnification = 6.3×; Leica Wild MZ8).
The percentage cover of target groups was estima-
ted by placing a transparent overlay, of 100 equally
spaced dots, on the pictures (10 ×14 cm) of the 12
‘micro’-quadrats. The values counted (i.e. percentage
cover of groups, see below) from these quadrats were
pooled to give a mean, which was used as a replicate
of the corresponding treatment. To minimize potential
edge effects, cover within 2 cm of the edge, or the
holes on the plates, was not included. Groups were de-
fined as: (1) CCA (mostly Hydrolithon samoënse,
‘Fosliella-state’ Hydrolithon sp. and Neogoniolithon
misakiense, but also sparse Lithophyllum sp.; see Hall-
Spencer 1994); (2) bleached coralline algae (i.e. dead
coralline algae); (3) Ralfsia spp.(brown crusts, mostly
R. expansa, but also sparse R. verrucosa); (4) non-
crustose macroalgae (including the green algae Ulva
spp. [mostly U. lactuca]; green turfs of Enteromorpha
compressa, Chaetomorpha antennina and Cladophora
delicatula; the brown algae Hincksia mitchelliae,
Colpomenia sinuosa and Endarachne binghamiae; the
red alga Gelidium pusillum; green spores); (5) sessile
animals (including the tube worms/spirorbid poly-
chaetes Spirorbis foraminosus and Hydroides elegans;
rock oysters Saccostrea cucullata and barnacles Bala-
nus amphitrite) and (6) bare surface.
Four-way analysis of variance (ANOVA) was used to
test for differences between years (2 levels; orthogonal
& random), seasons (2 levels; orthogonal & fixed), pools
(3 levels; orthogonal & random) and treatments (3 le-
vels; orthogonal & fixed) and also any interactions
between these factors after 4 mo of colonization/settle-
ment (i.e. data from October 2000 and 2001, summer,
and March 2001 and 2002, winter), followed by Stu-
dent-Newman-Keuls (SNK) multiple comparisons for
significant results (Underwood 1997). Cochran’s test
was performed to test for homogeneity of the data, and
data were transformed if necessary (Underwood 1997,
see Table 2 legend). As the abundance of Ralfsia spp.
and erect macroalgae was < 5 % in winter and summer,
respectively, these data were subject to a 3-way
ANOVA, to determine differences between years,
pools and treatments in summer for Ralfsia spp. and in
winter for erect macroalgae, when they were more
abundant.
Persistence of crustose coralline algae in space and
time. Experimental design: Algal-colonized PVC
plates were used to mimic the natural substrate as: (1)
this standardizes the substrate and provides a uniform
and repeatable sampling unit and (2) the colonization
history of the natural substrate in different pools is
not known (Smith et al. 2001). To prepare coralline-
colonized substrates, new, roughened PVC plates (as
described above) were introduced into pools for 5 mo
prior to the experiment to achieve >70% colonization
(similar to the natural rock in the pools). Plates were
then transferred to 3 different experimental pools for
1 mo before grazers were excluded (with appropriate
controls, as described above) using 3 treatments in
winter (December 2001 to April 2002) and in summer
(June 2002 to October 2002).
Sampling protocol and data analysis: Sampling and
counting methods were the same as above, except that
3-way ANOVA was used to determine whether there
were any differences between seasons, pools and
treatments and also whether there were any interac-
tions between these factors, after 4 mo of coloniza-
tion/settlement. Data subjected to analyses were the
differences in percentage cover before, and 4 mo after,
treatment installation (i.e. values could be positive or
negative). As the abundance of erect macroalgae was
<5% in summer, these data were subjected to a 2-way
ANOVA to determine differences between pools and
treatments in winter only.
Grazing pressure. In both experiments, sea urchin
grazing pressure was estimated from star-shaped
graze marks on the macro-photo-quadrats. The per-
centage cover of urchin marks was estimated by pla-
cing a transparent overlay, consisting of 100 equally
spaced dots, on the developed pictures (10 ×14 cm).
The grazing pressure of the most abundant gastropods
101
Mar Ecol Prog Ser 326: 99–113, 2006
was monitored using wax discs (see Wai &
Williams 2006 for details). Wax discs
(25 mm diameter) were cut from dental
wax sheets (0.25 mm thick, Gusswachs),
and 8 were evenly stuck onto a PVC plate
(16 ×8 ×0.4 cm) by heating in an oven
(52°C for ~15 to 20 min). Records of radula
and graze marks were obtained from
scanning electronic microscope (SEM)
images of these specimens and used as a
reference to identify marks on the wax
discs in the pools.
PVC plates with wax discs were screwed
around the top of each pool and left for 3 to
4 d on 3 randomly chosen dates in summer
and winter. The percentage cover of grazer
marks of individual species on each disc of
each plate was scored as the number of
dots of a 100 dot transparent overlay lying
over scratches of each species under a
binocular microscope (6.3×). As small-
scale, within-plate differences were not of
interest, the mean percentages of the cover
of marks on the 8 discs were pooled and
treated as a replicate in each pool. To pro-
vide background information about which
herbivore species grazed in the pools, the
overall grazing pressure in each pool, at
each sampling period, was standardized as
percentage cover per 3 d (more detailed
results are reported in Wai & Williams
2006). To estimate grazing pressure in the
primary settlement experiment, 12 plates
were deployed in Pools 1, 4 and 6 (n =
2 seasons ×3 pools ×3 dates ×12 plates
= 216), whereas only 8 plates were used in
the second experiment to investigate coral-
line persistence (n = 2 seasons ×3 pools
×3 dates ×8 plates = 144), as grazing pres-
sure was less variable in Pools 5, 8 and 9
(Wai 2004).
RESULTS
Primary algal settlement
In general, algal settlement patterns
were strongly affected by grazing in all
pools, but the rate of settlement and assem-
blage development varied spatially and
temporally. Bare space diminished in all
treatments as algae colonized and grew,
and this reduction was usually faster in
winter than in summer (Fig. 1), mainly as a
102
Fig. 1. Mean (+SD, n = 4) percentage cover of bare surface on new PVC
plates among different treatments (Cage: grazer exclusion, – grazers;
Fence: cage control, +grazers; Open: treatment control, +grazers) and
pools (1, 4 and 6) during summer (1st year: 2000; 2nd year: 2001) and
winter (1st year: 2000-01; 2nd year: 2001-02)
Wai & Williams: Effect of grazing on coralline algae
result of CCA settlement (Fig. 2, Tables 2
& 3). In contrast, the crustose algae Ralfsia
spp. and non-crustose macroalgae mostly
developed on grazer-exclusion plates (Figs. 3
& 4). CCA were the first crustose algae to
colonize, followed by Ralfsia spp. (and also a
very sparse, <1%, cover of green turfs and
Hincksia mitchelliae) in summer (Fig. 3)
and by non-crustose macroalgae in winter
(Fig. 4). Sparse cover (<1%) of sessile animals
(mostly Spirorbis foraminosus and sparse
Hydroides elegans, rock oysters Saccostrea
cucullata and barnacles Balanus amphitrite)
were also recorded.
Colonization extent. The extent of colo-
nization by algae varied with pool, season
and year (Table 2). Bare surface cover de-
creased faster in winter than summer in both
years. Patterns were similar in both winters,
whilst the summers varied, with a slower
algal colonization period in the second than
the first year (Fig. 1). Although overall trends
were similar between pools, the timing and
extent were variable (Fig. 1).
After 4 mo, higher bare surface cover was
left on the plates in summer than winter,
especially in grazer exclusions, in all pools.
This pattern was only significant in the sec-
ond year (Tables 2 & 3, Fig. 1), whereas in the
first year the bare surface cover was similar in
summer and winter. Pool 1 was, however, an
exception, where bare surface cover was
higher in winter in the first year, especially
in grazer-access treatments (Tables 2 & 3,
Fig. 1).
Crustose coralline algae. Whilst there was
a predictable, general pattern of CCA settle-
ment in all pools, the rate of settlement and
subsequent lateral growth varied with pool,
season and year (Figs. 1 & 2). Early settlement
of CCA (the number of settlers after the first
month) varied with treatment, pool, season
and year and significant interactions between
these factors (Table 2). CCA settlement rates
were higher in winter than summer in both
years (Table 3). Settlement rates between
treatments were similar in both seasons and
years, with the exception of the summer of
the second year (Table 3).
The colonization (settlement and develop-
ment) of CCA was higher in winter than sum-
mer in both years. CCA colonization was,
however, variable between pools in both
summer and winter of both years (Fig. 2). Col-
onization in the summer of the second year
103
Fig. 2. Mean (+SD, n = 4) percentage cover of crustose coralline algae on
new PVC plates among different treatments, pools, seasons and years.
See Fig. 1 for abbreviations
Mar Ecol Prog Ser 326: 99–113, 2006
was, in general, slower than that in the
first year (Fig. 2). After 4 mo, in both
seasons and years, CCA dominated
both open and fence treatments. Per-
centage cover varied with pools and
seasons/ years, in addition to the treat-
ment effect (Table 2) being, in general,
higher in grazer-access treatments than
exclusions (Table 3, Fig. 2). Bleached
coralline algae occurred in all pools in
August 2000 and October 2001 (Fig. 3).
Non-coralline algae. Ralfsia spp.
showed a relatively predictable settle-
ment pattern in all pools, but the rate and
cover varied with treatment, pool and
year. Both the settlement rate and cover
of Ralfsia in all pools were much higher
in summer than winter. In summer of the
first year, Ralfsia was abundant in grazer
exclusions, but not in all pools (Fig. 3). In
the second year, however, the overall
settlement rate and cover were much
lower in all pools (Fig. 3).
After 4 mo, in all pools, cover of Ralf-
sia in the first year was higher than in
the second year (Fig. 3). Ralfsia was
104
Source df Bare Number Crustose Fvs:
surface of coralline coralline
settlers algae
(70.45) (0.07) (99.19)
Ye 1 88.66* 0.04 2.37 Ye ×Po
Se 1 No test
Po 2 13.97* 6.29 16.74 Ye ×Po
Tr 2 No test
Ye ×Se 1 4.37 0.41 0.87 Ye ×Se ×Po
Ye ×Po 2 0.42 8.33*** 1.71 Residual
Ye ×Tr 2 5.52 0.47 0.88 Ye ×Po ×Tr
Se ×Po 2 1.13 0.51 3.84 Ye ×Po ×Tr
Se ×Tr 2 No test
Po ×Tr 4 1.05 5.53 8.83 Ye ×Po ×Tr
Ye ×Se ×Po 2 12.85*** 10.32*** 0.41 Residual
Ye ×Se ×Tr 2 1.59 0.17 10.85* Ye ×Se ×Po ×Tr
Ye ×Po ×Tr 4 1.01 1.65 3.03* Residual
Se ×Po ×Tr 4 3.48 1.29 2.52 Ye ×Se ×Po ×Tr
Ye ×Se ×Po ×Tr 4 0.86 3.45* 1.66 Residual
Residual 108
Table 2. F-ratios from ANOVA to investigate variation in percentage cover of
bare surface, crustose coralline algae and number of coralline settlers on new
PVC plates after 4 mo primary settlement between treatments (Tr), pools (Po),
seasons (Se) and years (Ye). Percentage cover data were arcsine (x%) trans-
formed, and the number of coralline settlers were ln(x+1) transformed. Cochran’s
test for homogeneity, p > 0.05. Values in parentheses are error mean squares.
Significant differences are given in bold and indicated by asterisk(s): *p <
0.05, ***p < 0.001. See Table 3 for results of Student-Newman-Keuls (SNK) tests
Fig. 3. Mean (+SD, n = 4) percentage cover of Ralfsia spp. and bleached corallines on new PVC plates in summer among differ-
ent treatments, pools and years. See Fig. 1 for abbreviations. Note scales of y-axis are different
Wai & Williams: Effect of grazing on coralline algae
usually most abundant in grazer exclusions, especially
during the first summer (Table 4, Fig. 3). The effect of
grazer exclusion did, however, vary with pools and
also with year. In the first year, Ralfsia cover, for exam-
ple, was higher in exclusion than in grazer-access
treatments in Pool 4, while in Pool 6 delayed settlement
resulted in a relatively lower cover in exclusions (Fig.
3). In addition, there was unexpectedly high Ralfsia
cover in the fence treatment in Pool 1 (but not in Pools
4 and 6) in summer of the first year (Table 4, Fig. 3). In
the second year, however, cover in all pools was much
lower than in the first year and grazer exclusion only
had an effect in Pool 1 (Table 4).
There was a strong seasonal trend in non-crustose
macroalgal settlement and growth, as most were only
found in winter, but cover varied with treatment, pool
and year (Table 4). Non-crustose macroalgae were al-
most only found in grazer exclusions in winter in both
years, although patterns and species compositions
varied between pools. In Pools 4 and 6, Hincksia mit-
chelliae rose to ca. 10% cover after 3 mo in
Year 1 and to ca. 20–30% cover after 3 mo in
Year 2. Green turfs peaked after 4 mo in
both years (30 to 40% cover), and Ulva spp.
rose to 5–15% cover in Year 1, but was
absent in Year 2. Colpomenia sinuosa was
virtually the only non-crustose alga to
appear in Pool 1 and peaked at 60 to 70%
cover after 2 mo in Year 1 and after 2 to 4 mo
in Year 2, before declining. Once these erect
macroalgae settled, they grew quickly, and
their increase was linked with a reduction in
visible CCA after 3 mo (Figs. 2 & 4). CCA,
however, persisted under the C. sinuosa,
and their percentage cover increased once
the C. sinuosa died. In both years, there was
a significant grazer-exclusion effect in all
the pools (Table 4), with erect algae being
confined to grazer exclusions apart from the
appearance of C. sinuosa in the fence treat-
ment in Year 1 and in open treatments in
Pool 1 in Year 2 (Fig. 4).
Grazing pressure in primary settlement
pools (1, 4 and 6). Graze marks of the
gastropods Chlorostoma argyrostoma, Lu-
nella coronata and Nerita albicilla were
abundant in all pools. Individual species
showed different patterns that were consis-
tent in all pools. Grazing pressure of L. coro-
nata, for example, was similar in both sum-
mer and winter, whilst N. albicilla and C.
argyrostoma exhibited seasonal variation. In
summer, grazing pressure of N. albicilla and
L. coronata was greater than that of C. a-
rgyrostoma in all pools (Fig. 5). In winter,
the grazing pressure of C. argyrostoma increased,
whilst that of N. albicilla was dramatically reduced.
Grazing pressure of the sea urchin Anthocidaris
crassispina was variable between pools, especially in
winter, with urchins removing between 9 and 78% of
the CCA in Pool 1, compared to 6 26% in Pools 4 and
6. Sea urchins, in general, grazed patchily, both in
space (large SD; Fig. 6) and time (large differences be-
tween months, e.g. in Pool 1; Fig. 6).
Persistence of crustose coralline algae in space and
time
Before treatment installation, CCA dominated the
surface of all plates (>70%; Fig. 7) and resembled the
surrounding assemblages (Wai 2004). After treatment
installation, a predictable pattern of secondary settle-
ment and development of algal assemblages was re-
corded. The persistence of CCA and final algal as-
105
SNK tests 1st year 2nd year
Bare surface:
Ye×Se ×Po:
Pool 1 Summer < Winter Summer > Winter
Pool 4 Summer = Winter Summer > Winter
Pool 6 Summer = Winter Summer > Winter
Number of coralline settlers:
Ye×Se ×Po ×Tr:
Summer Pool 1 Cage = Fence = Open Cage > Fence = Open
Pool 4 Cage = Fence = Open Cage < Fence = Open
Pool 6 Cage = Fence = Open Cage < Fence = Open
Winter Pool 1 Cage = Fence = Open Cage = Fence = Open
Pool 4 Cage = Fence = Open Cage = Fence = Open
Pool 6 Cage = Fence = Open Cage = Fence = Open
Pool 1 Cage Summer < Winter Summer < Winter
Fence Summer < Winter Summer < Winter
Open Summer < Winter Summer < Winter
Pool 4 Cage Summer < Winter Summer < Winter
Fence Summer < Winter Summer < Winter
Open Summer < Winter Summer < Winter
Pool 6 Cage Summer < Winter Summer < Winter
Fence Summer < Winter Summer < Winter
Open Summer < Winter Summer < Winter
Crustose coralline algae:
Ye×Po ×Tr:
Pool 1 Cage = Fence < Open Cage < Fence = Open
Pool 4 Cage < Fence = Open Cage < Fence = Open
Pool 6 Cage < Fence = Open Cage < Fence = Open
Ye×Se ×Tr:
Cage Summer < Winter Summer = Winter
Fence Summer < Winter Summer < Winter
Open Summer = Winter Summer < Winter
Summer Cage < Fence < Open Cage Open Fence
Winter Cage = Fence = Open Cage < Fence = Open
Table 3. SNK tests to investigate significant fixed factors from ANOVA
presented in Table 2 (see Table 2 for abbreviations)
Mar Ecol Prog Ser 326: 99–113, 2006
semblage development, however, var-
ied spatially and temporally and were
strongly affected by grazing in all
pools.
Crustose coralline algae, bleached
corallines and bare surface. In sum-
mer, there was a heavy mortality of
CCA from May 2002 to July 2002. In
July 2002, only ~20 to 30% CCA cover
remained (Fig. 7) and this was consis-
tent for all treatments and in all pools.
The extent of subsequent re-coloniza-
tion of CCA after July 2002, however,
varied with treatments and pools.
Cover gradually increased after Au-
gust 2002 in all grazer-access treat-
ments, but there was little recovery in
exclusion treatments. CCA were the
first encrusting algae to colonize newly
released PVC surfaces following the
summer die-off, followed by sparse
Ralfsia cover (<1%; Fig. 8) and green
spores (<5%) in October 2002.
The increase in cover of CCA in
grazer-access treatments was coupled
with a reduction in bare surface after
August 2002 or September 2002
(Fig. 7). In contrast, bare surface cover in grazer
exclusions continued to increase, except in Pool
8, where there was an increase in CCA cover
(Fig. 7). After the heavy summer bleaching and
mortality of CCA, the rate of release of bare sur-
face was much slower in grazer-exclusion than
grazer-access treatments and was consistent in
all pools (Fig. 7).
In winter, CCA cover gradually decreased after
treatment installation, the extent of which varied
between treatments, but was greater in grazer
exclusions and was coupled with an increase in
bare surface in the open and fence treatments
(Fig. 7) and cover of non-crustose macroalgae
(mainly green turfs; Figs. 7 & 9).
After 4 mo, CCA showed significant interactions
between pool and season, with greater cover in
summer than winter in some, but not all, pools
(Table 5). Cover decreased after 4 mo post-treat-
ment installation, reaching lower levels in summer
than winter in Pools 8 and 9 (Fig. 7). Bleached
CCA also showed a significant Se ×Po interaction
after 4 mo, with lower cover in summer than win-
ter in all pools (Table 5). Bleaching was most obvi-
ous in exclusions, where it peaked early in
summer (~60% cover), but increased progres-
106
Source df Ralfsia spp. Non-crustose macroalgae Fvs:
(0.58) (52.84)
Ye 1 17.87 3.35 Ye ×Po
Po 2 32.21 9.49 Ye ×Po
Tr 2 No test
Ye ×Po 2 4.20* 0.82 Residual
Ye ×Tr 2 2.74 0.21 Ye ×Po ×Tr
Po ×Tr 4 0.86 17.67 Ye ×Po ×Tr
Ye ×Po ×Tr 4 3.33* 4.17** Residual
Residual 54
SNK tests: 1st year 2nd year
Ralfsia spp.:
Ye×Po×Tr:
Pool 1 Cage = Fence > Open Cage > Fence = Open
Pool 4 Cage > Fence > Open Cage = Fence = Open
Pool 6 Cage > Fence = Open Cage = Fence = Open
Non-crustose macroalgae:
Ye×Po ×Tr:
Pool 1 Cage > Fence = Open Cage = Open > Fence
Pool 4 Cage > Fence = Open Cage > Open = Fence
Pool 6 Cage > Fence = Open Cage > Fence = Open
Table 4. F-ratios and SNK tests from ANOVA to investigate variation in percentage
cover of Ralfsia spp. and non-crustose macroalgae on new PVC plates after 4 mo
primary settlement between treatments (Tr), pools (Po), seasons (Se) and years
(Ye). Data were ln(x+ 1) and arcsine (x%) transformed, respectively. Cochran’s test
for homogeneity, p >0.05. Values in parentheses are error mean squares. Signifi-
cant differences are given in bold and indicated by asterisk(s): *p < 0.05, **p < 0.01
Fig. 4. Mean (+SD, n = 4) percentage cover of non-crustose
macroalgae on new PVC plates in winter among different treat-
ments, pools and years. See Fig. 1 for abbreviations
Wai & Williams: Effect of grazing on coralline algae
sively in winter (to 30 60% cover; Fig. 8).
Bare surface cover showed significant
interactions (Se ×Tr and Se ×Po; Table 5),
with greater cover in summer than winter
in grazer exclusions, but similar cover in
summer and winter in grazer-access treat-
ments (Table 5). At the end of summer,
bare surface cover was higher in exclu-
sions than in grazer-access treatments, but
this was not the case at the end of winter
(Table 5).
Non-coralline algae. Low cover (<5%)
of Ralfsia spp. was found in both summer
and winter (Fig. 8). Non-crustose macroal-
gal cover was virtually limited to winter in
all pools. A large proportion (90 to 100%)
of the non-crustose macroalgae were
green turfs (mostly Enteromorpha com-
pressa, but also Chaetomorpha antennina
and Cladophora delicatula); the rest (2 to
8%) comprised the brown alga Hincksia
mitchelliae. Only the green turfs were able
to overgrow the live coralline crusts (Wai
pers. obs.). H. mitchelliae only invaded at a
later stage, after new substrate was
released due to coralline bleaching. These macroalgae
were only occasionally recorded in summer, and the
percentage cover was very low (< 5%).
The pattern of macroalgal settlement was predict-
able in all pools, although the extent varied with treat-
ment and pool. Erect macroalgae were only able to
grow in grazer exclusions in winter, although sparse
new settlement and recruitment (< 2%) were found on
all plates in some pools prior to treatment installation
(i.e. December 2001; Fig. 9).
After 4 mo, macroalgae cover in exclusions was
greater than in grazer-access treatments (2-way
ANOVA, treatment effect, F2, 27, p =0.002, all other
terms p >0.05; followed by SNK tests, Cage > Fence =
Open treatments; Fig. 9), although settlement patterns
varied between pools. Macroalgae (i.e. green turfs)
grew quickly, although cover varied between pools,
with peak cover occurring at different times (Fig. 9).
The increase in cover of macroalgae in the grazer
exclusions was usually coupled with a reduction in
CCA cover after 1 mo (i.e. January 2002; Figs. 7 & 9).
Green spores were found in both summer and winter,
mostly at the latter stages of the experiments, but only
in grazer exclusions, where they reached 1 to 9%
cover.
Grazing pressure in the persistence experiment
pools (5, 8 and 9). Wax plates recorded abundant graze
marks of Nerita albicilla, Lunella coronata and
Chlorostoma argyrostoma in all pools. In both summer
and winter, grazing pressure of N. albicilla and L. coro-
107
Fig. 6. Anthocidaris crassispina. Mean (+SD, n = 8) percent-
age cover of graze marks by sea urchins on PVC plates. Note
scales of y-axis are different
Fig. 5. Chlorostoma argyrostoma, Lunella coronata and Nerita albicilla.
Relative percentage cover of graze marks (%; n = 36 for Pools 1, 4 and 6;
n = 24 for Pools 5, 8 and 9) of the most abundant gastropod grazers on wax
plates in different pools, during summer and winter
Mar Ecol Prog Ser 326: 99–113, 2006
nata was relatively greater than that of C.
argyrostoma in all pools (with the exception
of Pool 5 in winter; Fig.5). Although grazing
pressure of individual species varied with
season, there was no clear pattern. Sea
urchin grazing trails were only occasionally
found on grazer-access plates (see Wai
2004).
DISCUSSION
Factors affecting algal settlement patterns
and persistence in rock pools
CCA dominated all low-shore rock pools
during both summer and winter, but only in
the presence of natural herbivore densities.
Once a newly created bare surface was
available, CCA were always the first algal
crusts to colonize (also see Coleman 2003).
The persistence of CCA was, however,
strongly affected by physical (i.e. heat stress)
and biological (i.e. herbivore-induced/gra-
zing) disturbance and the interaction
between these factors. Such disturbances
play an important role by frequently renew-
ing rock space, in the form of discrete bare
patches within the corallines (see Paine &
Levin 1981, Sousa 1985), resulting in patches
of CCA at various stages of development (i.e.
a mosaic of different ‘ages’; Sousa 1985,
Benedetti-Cecchi & Cinelli 1994). In addi-
tion, grazer-mediated disturbance eliminates
competitively dominant epiphytic species
(Paine 1984), such as green algal turfs,
allowing a mosaic of coexisting, resilient
coralline species to persist in the pools.
Physical disturbance — heat stress during
summer
Many species of algae in rock pools, espe-
cially CCA, bleach when subject to heat
stress (Dethier 1984). Heat stress, resulting
from prolonged, daytime, spring low tides in
summer (pool water temperatures >30°C,
especially the top 30 cm), was an important
factor affecting coralline persistence. Mass
mortality and subsequent bleaching of
coralline algae, especially individuals that
settled in the previous winter (Wai 2004),
were common in all pools during the onset of
summer (~June).
108
Fig. 7. Mean (+SD, n = 4) percentage cover of crustose coralline algae and
bare surface on CCA-colonized PVC plates among different treatments
(Cage: grazer exclusion, –grazers; Fence: cage control, +grazers; Open: treat-
ment control, +grazers) and pools (5, 8 and 9), during summer and winter.
Note scales of y-axis are different
Wai & Williams: Effect of grazing on coralline algae
The rate and extent of coralline recovery,
however, varied between pools, indicating
differences in rates of settlement and recruit-
ment between pools and/or differences in
the extent and scale of disturbance (e.g.
grazing pressure, thermal stress; Chapman
& Underwood 1998). Between-pool differ-
ences in the timing and rate of settlement
may reflect highly localized sources of
propagules, suggesting that small spatial
scale variation is important in determining
pool assemblages (see Chapman & Under-
wood 1998).
In general, the turnover time needed for
CCA in summer (i.e. recovery or re-coloniza-
tion and return to initial cover, i.e. ~70%,
after disturbance induced by thermal stress)
was variable between pools (ranging from 2
to >3 mo) and with size of disturbed patches.
Maximum recovery rate was estimated to be
~17% cover mo–1 or 23.8 cm2mo–1, which is
sufficient to ensure the dominance and per-
sistence of CCA in these rock pools (also see
Adey & Vassar 1975, Johansen 1981).
Herbivore-induced disturbance in
low-shore rock pools
During the early settlement stage, al-
though CCA settlers were observed on new
surfaces in either the presence or absence of
macrograzers, CCA could only develop and
dominate the surfaces in the presence of
macrograzers. When macrograzers were
excluded, the later colonists, particularly
non-crustose macroalgae in winter and Ralf-
sia spp. in summer, overgrew the CCA.
Sea urchins are the dominant grazers, in
terms of their size and excavating ability, in
many intertidal and subtidal habitats (see
Lawrence 1975, Ayling 1981, Steneck &
Watling 1982). In this study, although the
density of sea urchins in some of the pools
and their corresponding grazing frequency
were low, their excavating ability and poten-
tial impact was relatively high as compared
to molluscan grazers (Spencer 1992). Sea
urchin grazing trails were often found (Wai
2004) and once they accessed substrates,
they created new patches of bare space in
between the developed CCA. This kind of
localized disturbance is common on rocky
substrates, with discrete patches of newly
created bare surfaces between existing
109
Fig. 8. Mean (+SD, n = 4) percentage cover of Ralfsia spp. and bleached
corallines on CCA-colonized PVC plates among different treatments
and pools, during summer and winter. See Fig. 7 for abbreviations.
Note scales of y-axis vary
Mar Ecol Prog Ser 326: 99–113, 2006
assemblages of different sizes and ages (Paine & Levin
1981, Sousa 1984, 1985). Such patches are important to
the success of primary colonists, such as coralline
algae, as these species perform lateral vegetative
growth and space is often a limiting resource (Sousa
1985, Steneck 1986).
Molluscan macrograzers were common in the pools
and were also able to remove algal biomass, and thus act
as a biotic disturbance (Steneck & Watling 1982, Wai &
Williams 2006). Although the excavating ability of indi-
vidual molluscan grazers is much more limited than that
of sea urchins (Spencer 1992), their combined grazing
pressure, in terms of disturbance frequency, was much
higher than that of sea urchins (Wai & Williams 2006).
These molluscan grazers may play a different role in
these algal assemblages, by exerting indirect effects on
the crusts, removing epiphytes or new recruits of more
competitive species (e.g. Ralfsia spp., filamentous green
turfs and erect macroalgae) or fouling materials (e.g.
sediments; Steneck et al. 1991, Hawkins et al. 1992).
Grazing may also help to release propagules from the
conceptacles of coralline algae and to enhance the avail-
ability of new recruits, facilitate subsequent settlement,
or stimulate productivity (Kaehler & Froneman 1999, Wai
& Williams 2005). Such algae– grazer interactions sug-
gest a positive relationship (i.e. mutualism) be-
tween grazers and encrusting algae and are
thought to be important for the success of
coralline crusts (Steneck 1986).
Macroalgae overgrew the CCA rapidly in
the absence of grazers. A variety of macroalgal
taxa (including Hincksia mitchelliae,
Enteromorpha compressa, Ulva spp., Colpo-
menia sinuosa and Gelidium pusillum) over-
grew newly settled CCA, whereas green turfs
(mostly E. compressa) were more readily able
to overgrow established CCA. The timing
and settlement rate of these erect macroal-
gae were, however, variable between pools.
These differences may be due to variability in
availability of algal propagules in different
pools and/or at different times, since even a
small difference in the timing of release of new
substrate may determine which algae can col-
onize the substrate (Figueiredo et al. 1997,
Chapman & Underwood 1998).
Deposition and accumulation of sediments
occurred amongst the turfs (see also Airoldi
& Virgilio 1998), which may also have had a
negative effect on the persistence and sur-
vival of the CCA (Fabricius & De’ath 2001).
Although some studies have shown that CCA
can persist underneath turfs (Airoldi 2000),
in the present study, most corallines were not
able to persist underneath the green turfs,
although they were able to persist for longer under C.
sinuosa.
Spatial and temporal variation
Settlement and cover of both CCA and erect macro-
algae varied between pools and seasons. All pools
were dominated by CCA, but each pool showed its
own specific algal settlement rates, highlighting indi-
vidual variability and the difficulties in generalizing
about the exact processes important in each pool
(Dethier 1984, Underwood & Jernakoff 1984). The pool
variation in settlement rates and species compositions
was probably related to the physical characteristics
of individual pools. The lower position of Pool 1, for
example, may favour faster rates of algal settlement for
CCA and Colpomenia sinuosa.
Variation in the supply of algal propagules may ex-
plain the patterns of recruitment of algae, both spatially
(Andrew & Viejo 1998) and temporally (Sousa 1985,
Benedetti-Cecchi & Cinelli 1994). Macroalgal distribu-
tion and abundance in Hong Kong show strong seasonal
variation (Hodgkiss 1984, Williams 1993, Kaehler &
Williams 1996). The persistence of CCA (Wai 2004),
110
Fig. 9. Mean (+SD, n = 4) percentage cover of non-crustose macroalgae
on CCA-colonized PVC plates among different treatments and pools,
during summer and winter. See Fig. 7 for abbreviations
Wai & Williams: Effect of grazing on coralline algae
however, implies that seasonal variation does not play
such an important role in the low-shore rock pools.
CCA did, however, show seasonal differences in
settlement rate and in the species recorded (also see
Hall-Spencer 1994). In winter, corallines colonized bare
surfaces and grew at a faster rate than in summer (~1 to
2 mm mo–1; Wai 2004, especially Hydrolithon samoënse
and Neogoniolithon misakiense), probably as a result of
the cooler water temperature (mean < 20°C). Patches
that settled in winter were often bleached during early
summer. Bleached corallines oc-
curred in all pools in summer, prob-
ably due to increased pool water
temperatures during daytime,
spring low tides (max. emersion pe-
riod >10 h during calm days). All
the bleached corallines died and
sloughed off the substrate. In addi-
tion to heat stress, pulses of lower
salinities (< 26 ‰) in summer after
heavy rain during low tide can also
be a potential cause of bleaching
(also see Morritt & Williams 2000).
The salinity of open seawater re-
corded during summer (< 28‰) was
generally lower than in winter
(>32‰) and, in 2001, salinities
< 25 ‰ were recorded, which may
explain the low settlement rate of all
algae, especially Ralfsia spp.
The increase of Ralfsia in summer,
but not in winter, indicated summer
was favorable for its growth or re-
production. Ralfsia settlement, how-
ever, varied between pools and
years. Other erect macroalgae like
Enteromorpha compressa, Ulva spp.
and Colpomenia sinuosa are ephe-
meral and only able to reproduce/
grow rapidly in winter. This strategy
of fast growth is important for the
success of these species, as, once
they settle and escape from grazing,
they grow to a large size and occupy
a substantial area of substrate
within a short time (e.g. C. sinuosa).
This rapid growth also explains why
some macroalgae, such as C. sinu-
osa, were also found in open/fence
treatments (i.e. grazer-access sub-
strates) in winter, as they can
achieve the necessary size to escape
from molluscan grazers.
Characteristics of crustose coralline algae in
low-shore rock pools
The dominance of CCA in pools suggests that these
slow-growing, competitively inferior, but grazer-resis-
tant algae are better adapted to these pool habitats
than other algae. The production of non-mobile propa-
gules, which is unique to the Rhodophytes (Graham &
Wilcox 2000), for example, is likely to enhance early
post-settlement attachment and survival of these pro-
111
Table 5. F-ratios from ANOVA to investigate change in percentage cover (before
and after 4 mo treatment installation) of crustose coralline algae, bleached coralline
algae and bare surface on CCA-colonized PVC plates after 4 mo between treat-
ments (Tr), pools (Po), seasons (Se) and years (Ye). Data were not transformed.
Cochran’s test for homogeneity, p >0.05. Values in parentheses are error mean
squares. Significant differences are given in bold and indicated by asterisk(s):
*p <0.05, **p < 0.01, ***p < 0.001
Source df Crustose Bleached Bare F vs:
coralline coralline surface
algae algae
(327.62) (137.43) (332.56)
Se 1 3.01 24.81* 1.37 Se ×Po
Po 2 1.09 2.03 3.98* Residual
Tr 2 26.62** 13.20* 3.96 Po ×Tr
Se ×Po 2 12.13*** 5.44** 4.47* Residual
Se ×Tr 2 2.02 2.95 7.69* Se ×Po ×Tr
Po ×Tr 4 1.78 1.51 0.97 Residual
Se ×Po ×Tr 4 0.53 1.12 1.21 Residual
Residual 54
SNK tests: means (SE), negative values indicate decline of percentage cover
after treatment installation
Crustose coralline algae:
Se ×Po: Tr:
Pool 5 Summer = Winter Cage < Fence = Open
–34.10 (6.40) –30.49 (8.29) –58.75 (4.23) –17.80 (5.86) –12.06 (4.89)
Pool 8 Summer > Winter
–3.01 (8.74) –47.26 (5.90)
Pool 9 Summer > Winter
–12.82 (10.42) –49.52 (8.28)
Bleached coralline algae:
Se×Po: Tr:
Pool 5 Summer < Winter Cage > Fence = Open
–7.90 (2.27) +16.03 (3.88) +20.33 (5.09) +2.55 (4.05) +1.15 (3.57)
Pool 8 Summer < Winter
–12.34 (5.15) +32.49 (3.90)
Pool 9 Summer < Winter
–3.91 (3.12) +23.66 (6.63)
Bare surface:
Se×Tr: Se ×Po:
Cage Summer > Winter Pool 5 Summer > Winter
+43.43 (6.34) +6.70 (2.09) +39.56 (6.42) +10.85 (5.24)
Fence Summer = Winter Pool 8 Summer = Winter
+13.56 (8.11) +17.85 (5.78) +12.25 (7.37) +8.94 (2.77)
Open Summer = Winter Pool 9 Summer = Winter
+10.40 (6.20) +10.92 (4.30) +15.57 (8.30) +15.68 (4.97)
Summer Cage > Fence = Open
+43.43 (6.34) +13.56 (8.11) +10.40 (6.20)
Winter Cage = Fence = Open
+6.70 (2.09) +17.85 (5.78) +10.92 (4.30)
Mar Ecol Prog Ser 326: 99–113, 2006
pagules (Vadas et al. 1992), especially when the pools
are uncovered by tides, and the calm water may facili-
tate these propagules to settle on substrates within the
same pools. CCA reproduce all year round (Steneck
1986, Hall-Spencer 1994, Williams et al. 1995), and
such a strategy allows rapid recruitment to occur once
new substrates become available. Such rapid recruit-
ment is important when the removal of adult biomass is
greater than lateral regeneration (Kaehler & Williams
1997). Fast re-colonization of newly released bare
space from disturbance was common in all pools. In
summer, the turnover rate of coralline cover on algal
established plates was ~3 to 4 mo, and patterns of set-
tlement and development were similar to those
observed on new bare surfaces. Although the persis-
tence of coralline algae relies on the grazing activities
of herbivores to remove epiphytes, their ability to sur-
vive and rapidly recover from both abiotic (i.e. heat
stress) and biotic (i.e. grazing pressure) disturbance
allows them to be successful colonists and to dominate
low-shore rock pools. This frequent disturbance and
re-colonization results in the typical mosaic of patches
of thin, newly settled CCA in between the developed,
thicker CCA seen in low-shore rock pools in Hong
Kong.
Acknowledgements. The authors thank their colleagues in
the Rocky Shore Ecology group (Department of Ecology &
Biodiversity, The University of Hong Kong) for their help in
the field; Prof. B. Darvell (The University of Hong Kong) for
providing us with dental wax; Dr. L. Benedetti-Cecchi for his
useful comments on statistical analyses; and the referees
whose comments helped improve the clarity of the manu-
script. This research was conducted in partial fulfillment of a
PhD degree by T.-C. Wai, who was supported by a post-
graduate studentship at The University of Hong Kong.
Permission to work at the Cape d’Aguilar Marine Reserve was
granted by the Agriculture, Fisheries and Conservation De-
partment, Hong Kong Government, HKSAR, China.
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Editorial responsibility: Otto Kinne (Editor-in-Chief),
Oldendorf/Luhe, Germany
Submitted: September 23, 2004; Accepted: March 29, 2006
Proofs received from author(s): October 11, 2006
... • the Royal Institute for Chartered Surveyors (RICS) guidelines for aerial survey • Methodologies to inform assessment of Good Ecological Status for UK rocky shore habitats for the Marine Strategy Framework Directive (Burrows et al., 2014) • MarClim methodology applied to investigation of the effects of climatic warming on marine biodiversity Mieszkowska et al. (2005;2006; • NRW Guidance GN006: Marine Ecology Datasets for marine developments and activities (Natural Resources Wales, 2019). Identifies data sources for intertidal habitat maps and provides information on the marine ecology data sets we hold and routinely use and how you can access them. ...
... reefs (see Sabellaria reef chapter GN030d), and Mytilus edulis beds that themselves are of conservation concern due to the important ecosystem services they provide (Davies & Newstead, 2013;Pearce et al., 2011;Seed et al. 2000). Furthermore, the rockpools that form in the holes and depressions of rocky shores act as nursery grounds (Horn & Martin, 1999), feeding habitat (Noël et al., 2009;Wai, 2006;Wai & Williams, 2006) and refugia (Schonbeck & Norton, 1978;Underwood & Jernakoff, 1984) for a wide range of organisms at low tide (Zander et al., 1999). They may also represent a key habitat underpinning coastal fish species diversity, as it is thought that almost all coastal fish species may, at some point or another in their lifetime, utilise rockpools (White et al., 2015). ...
... Quantitative records were taken for limpets, barnacles and trochids within various sizes of quadrats at each tidal height. See Mieszkowska et al. (2008;2006; for further details. The method continues to be used across the UK, with additional species added to the search list. ...
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Technical Report
This guidance document is one of a series of Benthic Habitat Assessment Chapters developed by Natural Resources Wales (NRW) for key habitats of conservation importance around Wales. It has been prepared by NRW with the initial document prepared under contract by APEM Ltdand Ocean Ecology Limited. The guidance aims to assist developers in designing and undertaking robust benthic habitat characterisation surveys and monitoring of these habitats in the context of Ecological Impact Assessment, thereby helping streamline the regulatory review and consultation process. This chapter will be relevant if you need to characterise and/or monitoring intertidal rocky shore and rockpool habitats. If you are unsure about the habitats present in the intertidal area youare interested in, you should consult existing information (see section 4.1) and/or you may need to carryout Phase 1 intertidal survey (section 5.1) to determine the habitats present before undertaking more focussed characterisation surveys.
... Therefore, we expect oscillation in the intensity of the physical and/or biological disturbance, allowing active growth of CRA, on the one hand, and their fragmentation, on the other. Because shallow waters are zones of high productivity and hydrodynamics, the grazing of fleshy algae on CRA thalli by herbivores and their mechanic fragmentation by water action is expected (Steneck 1986(Steneck , 1991(Steneck and 1994Wai and Williams 2006). This mechanism sufficiently explains the generation of biogenic material, as well as the absence of massive encrustations or large biogenic concretions. ...
... The first mentioned include two separate functional groups-thin and thick thalli (Steneck and Detheir 1994). In general, both geniculate and non-geniculate CRA are the first macrophytes colonising the free substrate (Wai and Williams 2006). In the mid-littoral and shallow littoral, the succession in CRA crusts consists of thin thalli overgrown by a thick one (Steneck 1986;Steneck et al. 1991;Adey and Vassar 1975). ...
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The studied transgressive deposits record the imprints of the coastal upwelling affecting the distribution of the shallow-water benthic assemblage in the early Priabonian Central Carpathian Paleogene Basin (CCPB). Our inferences are based on the study of benthic and planktonic assemblages, with special emphasis on the coralline algal (CRA) system, and the facies development at the Štrba locality. We have observed the development of cool-water carbonates on warm-water carbonate platforms. Coralline algal assemblage predominated through hapalidialids, rhodalgal and bryomol grain associations; specific microborings and calcareous nannoplankton in the Štrba locality are indicative of cool-water, while nummulite banks and hermatypic corals from adjacent and distant sites within the basin are indicative of warm-water carbonates. The last mentioned are indicative of oligotrophic and oligophotic settings, while nannoplankton, bryozoans and mollusks suggest mesotrophic conditions. Given the above, our results show the heterogeneous distribution of sea water temperature and nutrients that are characteristic for recent seasonal wind or eddy-driven coastal upwelling ecosystems (e.g. in the Mediterranean Sea). Upwelled cold and nutrient-enriched water enhanced the expansion of suspension feeders and favoured the growth of cool-water CRA with gametophytic phases. In the seasons without upwelling, nummulits could thrive in warm-water settings. This mechanism well explain why extensive nummulit banks were developed in adjacent sites but were not in the Štrba locality. The section is topped by bryozoan marlstone with glaucony. This lithofacies indicates the deepening of the basin. Here we were not able to discriminate between agents causing nutrification (e.g. upwelling, river plumes or gradual cooling) and the associated mesotrophication of the environment during the climatic deterioration documented across the CCPB.
... A recent survey from South African boulder shores reported one species (Spongites yendoi) (Tucker et al. 2017). Nongeniculate corallines commonly encrust shaded rock surfaces (Choi and Ginsburg 1983;Melville and Connell 2001 ;Connell 2003;Irving et al. 2004) and those exposed to direct sunlight (Wai and Williams 2006;Pacheco et al. 2010). They can extend far under shaded edges of boulders and sometimes to the very centre of the underside (Liversage 2016) despite extreme light limitation (K. ...
... Reproduction and settlement timing is variable; in the Mediterranean, the development of conceptacles containing reproductive organs occurred year round for one species but mostly during Autumn for another (Garrabou and Ballesteros 2000). Settlement and recruitment on a Hong Kong shore w ere strongest during winter months (Wai and Williams 2006). Once established, nongeniculate corallines can withstand severe conditions that displace many other species. ...
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Compared to stable reef habitats, dynamic boulder-reefs (commonly called boulder-fields when intertidal) host many habitat specialist species. Most occur underneath boulders where they are largely hidden from view; only limited research has assessed their life-histories despite their widespread importance for biological diversity. But some abundant under-boulder species likely structuring this system are habitat generalists widely researched elsewhere. Here we review this research, focusing on three widespread under-boulder sessile taxa: spirorbids, serpulids (tubeworms) and nongeniculate coralline algae, and three mobile taxa: sea urchins, chitons and crabs. Spirorbids have extensive reproductive/colonization capabilities but are readily out-competed. We thus characterize spirorbids as mostly early-successional, while serpulids often have greater competitiveness. Nongeniculate corallines occur underneath boulders where light reaches, although they can withstand low levels of that and most other resources. Such traits characterize nongeniculate corallines as late-successional. Thus, succession underneath boulders may shift deterministically from early tubeworms to late nongeniculate corallines. Habitat generalist sea urchin and chiton species often have strong inter-specific interactions in exposed habitats. Future experiments may find that under-boulder aggregations of these taxa, and also crabs, are impacting algal and invertebrate assemblages. These experiments will be required if dynamic boulder-reefs are to be as thoroughly understood as other benthic systems.
... Our experiments involving surface topography revealed that recruitment rates were greatly enhanced on more complex surfaces with irregularities on a scale of 100s of microns. Although we needed to use artificial substrata to manipulate this surface characteristic, coralline algae are able to settle on artificial surfaces (Steneck and Adey 1976, Harlin and Lindbergh 1977, Johansen 1981, Wai and Williams 2006, and surface characteristics have been shown to be important (Ogata 1953, Harlin andLindbergh 1977). The low number of surviving recruits on smooth surfaces, observed both on the putty patties and the smooth areas of the plates used in our second experiment, suggests that they were susceptible to grazing albeit other causes are possible (e.g., poor spore adhesion, mortality from desiccation). ...
... GRAZER-DEPENDENT RECRUITMENT OF CORALLINE ALGAE either by interfering with the settlement of spores or competing for resources. Similar explanations have been proposed for other observations of increased recruitment of coralline algae in the presence of grazers (Wai and Williams 2006) even including inconspicuous mesograzers such as small crustaceans (Bellgrove et al. 2014). ...
Article
Coralline algae are conspicuous members of many marine assemblages, especially those characterized by intense grazing pressure. We explored whether articulated species, especially Corallina vancouveriensis, depend on grazing invertebrates to both establish and flourish in an exposed rocky intertidal setting, and whether this plant-grazer relationship varied over more than three orders of magnitude (≈100 μm to >300,000 μm). Three experimental manipulations, supplemented by observations on recruitment, demonstrated that (1) C. vancouveriensis failed to recover rapidly from disturbed areas when grazers were experimentally excluded; (2) recruitment occurred in the presence of grazers; (3) increasing surface texture of molded surfaces enhanced coralline recruitment more when grazers were present; and (4) settlement occurred predominately in microtopographical low areas of a molded surface whereas a competitively superior fleshy red alga tended to recruit to high areas. These results confirm that coralline algal establishment and persistence are enhanced by grazers and reveal that this relationship is consistent over a range of biologically relevant scales. This article is protected by copyright. All rights reserved.
... Other CCA species (Lithothamnion glaciale) have shown tolerance to low salinity conditions, but as in our mesocosm studies, these studies were conducted on mature individuals (Burdett et al., 2015). However, further studies are needed to quantify and observe other factors such as grazing (Wai and Williams, 2006) and sedimentation (Wilson et al., 2004). ...
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In the Beaufort Sea, Arctic crustose coralline algae (CCA) persist in an environment of high seasonal variability defined by naturally low pH ocean water and high magnitude freshwater pulses in the spring. The effects of salinity on the CCA Leptophytum foecundum were observed through a series of laboratory and field experiments in Stefansson Sound, Alaska. We found that salinity (treatments of 10, 20, and 30), independent of pH, affected L. foecundum physiology based on measurements of three parameters: photosynthetic yield, pigmentation, and calcium carbonate dissolution. Our experimental results revealed that L. foecundum individuals in the 10-salinity treatment exhibited an obvious stress response while those in the 20- and 30-salinity treatments were not significantly different for three parameters. Reciprocal in situ transplants and recruitment patterns between areas dominated by CCA and areas where CCA were absent illustrated that inshore locations receiving large pulses of freshwater were not suitable for CCA persistence. Ultimately, spatially and temporally varying salinity regimes levels affected distribution of CCA in the nearshore Arctic. These results have implications for epilithic benthic community structure in subtidal areas near freshwater sources and highlight the importance of salinity in CCA physiology.
... At this time of the year, the encrusting algae also proliferate, with coralline algae growing rapidly to colonise the low-to mid-intertidal levels of semi-exposed shores (Williams, 1993b;Kaehler and Williams, 1996). Grazing by sea urchins (Anthocidaris crassispina) is important in the shallow subtidal, also affecting the algal assemblage on a seasonal basis (Wai and Williams, 2006). ...
... At this time of the 657 year the encrusting algae also proliferate, with coralline algae growing rapidly to colonize the 658 low to mid intertidal levels of semi-exposed shores (Williams, 1993b;Kaehler & Williams, 659 1996). Grazing by sea urchins (Anthocidaris crassispina) is important in the shallow subtidal, 660 also affecting the algal assemblage on a seasonal basis (Wai & Williams, 2006). ...
Full-text available
Chapter
Interactions in the Marine Benthos - edited by Stephen J. Hawkins August 2019
... We revealed that sea urchins are sensitive to the toxic effects of benthic dinoflagellates, potentially leading to impaired development and even death. Sea urchins are important herbivores in both coral (McClanahan et al., 1999;O'Leary and McClanahan, 2010) and rocky reefs (Andrew and Underwood, 1993;Tuya et al., 2005;Wai and Williams, 2006). Altering their population dynamics may have downstream consequences for the marine food chain and subtidal ecosystem including tropical coral reefs (Steneck, 1986;Carpenter and Edmunds, 2006;Littler and Littler, 2007) and temperate rocky reefs (Johnson and Mann, 1988;Elner and Vadas, 1990;Scheibling et al., 1999); and may potentially cause phase-shifts between alternate states (e.g. between coralline barren grounds and macroalgal beds on coral and rocky reefs; Steneck et al., 2002;Walker and Meyers, 2004;O'Leary and McClanahan, 2010). ...
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Coolia are marine benthic dinoflagellates which are globally distributed and potentially toxic. This study provides the first investigation of species diversity and toxicity assessment of Coolia in Hong Kong waters. Fifty-one strains of four Coolia species, including C. malayensis, C. canariensis, C. tropicalis, and C. palmyrensis, were isolated from twelve sub-tidal habitats, and identified phylogenetically using 28S rDNA sequences. Exposure experiments (48-hour) demonstrated that the algal lysates extracted from the four Coolia species exhibited different toxic effects on the lethality and abnormality of two invertebrate larvae, i.e., brine shrimp Artemia franciscana and sea urchin Heliocidaris crassispina. Heliocidaris crassispina was more sensitive to the toxic effects of Coolia species than A. franciscana. Toxicity tests from both larvae revealed that C. malayensis was generally more toxic, and caused higher mortality rates when compared with the other three species. The emerging threat of harmful benthic dinoflagellates to marine environments and sensitive biota is discussed.
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By measuring overgrowth patterns for the two most abundant tidepool species of crustose coralline algae (Lithophyllum impressum and Pseudolithophyllum whidbeyense) in the San Juan Islands, Washington State, the authors documented a reversal in competitive dominance that occurs at about the +1m level; L. impressum wins in upper zones, P. whidbeyense in lower zones. Regardless of tidepool elevation or species, thicker crusts overgrow thinner ones and crusts of equal thickness are competitively equal. Both crust species are grazed by limpets (primarily Lottia pelta and Tectura scutum); such grazing can reduce crust thickness. Corallines in tidepools in the upper intertidal zone are subject to high frequency (bite rate per unit area) and low intensity (penetration depth per bite) limpet grazing; those in low tidepools are subjected to opposite grazing characteristics. L. impressum is a thick crust, which has a multicellular covering over its meristem. This covering protects the growing tidepools. P. whidbeyense lacks a multilayered epithallus and is more susceptible to injury in high tidepools. In low pools meristems of both crusts are injured. L. impressum heals these deep wound by regenerating vertically, but the net result is a thinner plant that is easily overgrown. P. whidbeyense dominates the low zone because it is capable of much more rapid lateral growth including over its own deep wound. -from Authors
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Article
The species composition of pools in the intertidal zone on the coast of Washington State varies greatly from pool to pool and from time to time. While assemblages change somewhat predictably from the low- to the high-intertidal zone (presumably owing to different stress tolerances of the species), the variance among pools at a given tidal height cannot be ascribed to such physical factors. Some pools at each height are dominated by one species that monopolizes space on the rock or in the water column and modifies the pool environment. Each dominant species, once established, can spread rapidly through a pool (either by vegetative growth or by enhanced recruitment of its conspecifics) and is thus potentially self-perpetuating. When abundant, most dominants appear to prevent potential competitors from settling and surviving by monopolization of resources, abrasion of the substratum, and/or collection of sediment. Six such dominants were identified for Washington tidepools: from low to high pools, these are (1) the surfgrass Phyllospadix scouleri, (2) articulated coralline algae, (3) the mussel Mytilus californianus (exposed shores), (4) the cloning anemone Anthopleura elegantissima (more protected shores), (5) the red alga Rhodomela larix, and (6) the green alga Cladophora sp. Colonial diatoms also appear capable of dominating low pools in the absence of wave disturbance. However, each dominant monopolizes only 20-50% of the pools at any height. Disturbances, defined here as a loss of biomass exceeding 10% cover of a sessile species within 6 mo and caused by extrinsic forces, were observed frequently in regularly censused tidepools. Disturbance agents included waves, excessive heat, wave-driven logs or rocks, and unusual influxes of predators and herbivores. Severe disturbances (those affecting a large proportion of the organisms in a pool) tended to occur in high pools in the summer (due to heat stress) and low pools in the winter (due to wave damage). Overall, a disturbance occurred in every pool studied an average of every 1.6 yr. About half of the 231 observed disturbances affected one of the six dominant species. The frequencies of these disturbances ranged from one every 2-5 yr, and recovery of the species to its original level required 3 mo to > 2 yr. Some species (e.g., Rhodomela) were disturbed frequently bu recovered quickly because of rapid vegetative growth. However if asexual propagation was not possible, such as when the entire population of a species was removed from a pool, the slowness and irregularity of recruitment of sexual propagules greatly impeded recovery. Experimental manipulations involving the total removal of dominant species from pools showed that such large disturbances often require > 3 yr for recovery. The irregularity of planktonic recruitment can be compounded by the presence of herbivores, which can remove most settling organisms from the substratum, or by the absence of other organisms that are necessary for the settlement of a dominant (e.g., seed-attachment sites for Phyllospadix). The combination of high disturbance frequency and slow rates of recovery makes it impossible for any dominant to occupy all the pools in its tidal range at any one time. Disturbance is viewed in these habitats as the stochastic factor overlying other, more predictable, community-structuring factors such as tidal height, pool size, wave exposure, and levels of herbivory, predation, and competition. Thus combined deterministic processes and random events operate to produce a complex mosaic of species assemblages in pools in one region. None of the tidepool assemblages is @'stable@' over many generations; rather, they seem to exist in a dynamic state where disturbances are an integral structuring factor.
Article
Focuses on the effects of natural disturbance on the assemblages of sessile algae and invertebrates that occupy the surfaces of intertidal rocks. Space for attachment and/or resources associated with open substrates are usually the key limiting requirements. Organisms secure space by overgrowing or laterally crushing neighbours, by spreading vegetatively into open space, or by growing from settled propagules. Attributes of a newly created patch (eg surface characteristics, size, shape and location) can affect colonisation and subsequent interactions. Distinction is drawn between the creation of patches within already occupied sites and of those isolated from occupied sites. Characteristics of the disturbance regime are described, and modes of patch colonisation examined. Responses of mobile consumers to patch characteristics are discussed, within-patch dynamics are noted, and regional persistence of fugitive species is considered. -P.J.Jarvis
Chapter
Publisher Summary This chapter focuses on the aspects of stress in the tropical marine environment. There have been many studies of the tropical environment, many of them concerned with theories of the cause of the high speciation there; most of these have been focused on the land, and particularly the rain forest. The present study arises from the observation that it is much more difficult to keep organisms alive in the laboratory in the tropics than it is in temperate climates. Departure from optimal conditions for one environmental factor tends to reduce the tolerance range of a species for other factors. Throughout this chapter, the terms polar, temperate , and tropical have been used to refer to cold, intermediate, and warm seas without implying correspondence with well-defined zoogeographic regions. Physical aspects—such as temperature, salinity, radiation, and tides along with biological aspects—such as temperature tolerance, intertidal zonation, and critical levels—are discussed. The range of temperature tolerance is low in the tropics. Individual species there occupy a smaller fraction of the intertidal zone, and critical levels are shifted downwards. Tropical growth rates are high but very variable and there is less growth after sexual maturity than in mid-latitudes. The seasonal pattern of tropical growth is very variable. Longevity is less. The proportion of large species is less in the tropics, although there are some giant species there. Adaptation to the tropics may involve slowed growth, great size, and extended vertical intertidal range. Those species that show such adaptation are unable to live outside the tropics. These aspects seem to indicate that tropical seas are regions of increased stress.
Article
The colonization, taxonomic succession and marginal growth and accretion rates of crustose corallines on artificial substrates in algal ridge and reef environments on St Croix, U.S. Virgin Islands were examined . Very thin Leptoporolithon and Tenarea species are the initial colonizers of glass and plastic plates placed in these environments. In strong light conditions, the colonizers are followed by Neogoniolithon and Porolithon species. In areas of high wave energy, where the activities of grazing organisms are greatly reduced, the climax species Lithophyllum congestum and Porolithon pachydermum are capable of building intertidal algal ridges. The dominant coralline crusts showed marginal crustal extension rates of 0.9–2.3 mm/month and accretion rates of about 1–5.2 mm/year. Mean rates are about an order of magnitude greater than those previously measured in subarctic waters. The accretion rates are highly dependent upon the grazing activities of animals, especially parrot fish. Maximum rates in areas of minimum grazing are close to algal ridge accretion rates determined by C¹⁴ dating.