Coral Reefs (2001) 20: 255±262
DOI 10.1007/s003380100166
R EP O RT
Robert D. Sluka á Margaret W. Miller
Herbivorous ®sh assemblages and herbivory pressure
on Laamu Atoll, Republic of Maldives
Received: 30 June 2000 / Accepted: 20 April 2001 / Published online: 8 August 2001
Ó Springer-Verlag 2001
Abstract While herbivory is recognized as a fundamental process structuring coral reef communities, herbivore assemblages and processes are poorly described
for reefs in the Indian Ocean region. We quanti®ed
herbivorous ®sh assemblage structure (abundance and
diversity) in Laamu Atoll, Republic of Maldives, in four
reef habitat types: faro reef ¯ats, faro reef slopes, inner
and outer atoll reef slopes (20 sites in total). Herbivorous
®sh assemblages, representing a total of 30 species,
grouped strongly by habitat type, with the highest absolute abundance observed on faro reef ¯ats and lowest
abundance on inside atoll rim reef slopes. Removal of
Thalassia seagrass blades by ambient herbivore assemblages was used in a bioassay to assess relative herbivory
pressure among four habitat types (eight sites). Also, at
one site a choice herbivory assay was performed to
assess herbivore preference among four benthic plants
across three depth zones. Relative herbivory, as indicated by Thalassia assays, was highest on inside atoll rim
reef slopes and lowest on outside atoll rim reef slopes.
Thalassia consumption did not correspond to overall
herbivorous ®sh abundance, but corresponded more
closely with parrot®sh abundance. In the choice assays,
herbivores showed strong preferences among plant
Electronic supplementary material to this paper (Appendix 1) can
be obtained by using the Springer LINK server located at http://
dx.doi.org.1007/s003380100166.
R.D. Sluka
Oceanographic Society of Maldives,
P.O. Box 2075, MaleÂ, Republic of Maldives
M.W. Miller (&)
National Marine Fisheries Service,
Southeast Fisheries Science Center,
75 Virginia Beach Dr., Miami, Florida 33149, USA
E-mail: margaret.w.miller@noaa.gov
Tel.: +1-305-3614561
Fax: +1-305-3614562
Present address: R.D. Sluka
PHRA No. 12, Pothujanam Road, Kumarapuram,
Trivandrum, Kerala 695011 India
types and consumption of most plant types was higher
at mid-depth than in the shallow reef ¯at or deep reef
knoll zones.
Keywords Herbivory á Herbivorous ®shes á
Assemblage structure á Maldives
Introduction
Coral reefs are perhaps unique ecosystems in terms of
their high rates of primary production coupled with
extremely high rates of transfer of this primary production to primary consumers (Hatcher 1990). Hay
(1991) argues that this coupling of high production with
high consumption in tropical coral reefs makes plant/
herbivore interactions among the most important
structuring factors for these communities. A major
manifestation of herbivore control of benthic communities is the role that coral reef herbivory plays in mediating competition between fast-growing benthic algae
and relatively slow-growing corals (Miller 1998), allowing corals to ¯ourish by keeping macroalgal standing
crop limited to virtually nil.
A rich literature concerning herbivory on Caribbean
coral reefs has documented strong in¯uence by herbivores on benthic community structure via small-scale
experimental studies (Carpenter 1986; Lewis 1986;
Morrison 1988) and via the region-wide reduction in
herbivory after the 1983 epizoic die-o of a dominant
herbivore, Diadema antillarum (reviewed by Lessios
1988). There is some debate regarding possible anthropogenic (i.e. over®shing) in¯uence on the dominance
of urchins in herbivory processes in many Caribbean sites
studied in the 1970s and early 1980s (Hay 1984; Knowlton 1992; Jackson 1997). However, there is little doubt
that ®shes are the dominant herbivores on Caribbean
reefs since the Diadema die-o, as urchin recovery has
been minimal (but see Aronson and Precht 2000). Overall, ®shes on tropical coral reefs have high diversity,
high abundance, and high per capita consumption rates
256
relative to both temperate ®shes (Gaines and Lubchenco
1982) and invertebrate herbivores (Andrew 1989).
The in¯uence of herbivory in structuring Indo-Paci®c
reefs has received relatively less attention and most
published studies are restricted to Australia's Great
Barrier Reef (GBR) region. Comparisons of herbivory
and herbivorous ®sh communities in the GBR document
that nearshore reefs relative to oshore reefs show reduced in¯uence of herbivorous ®shes on benthic algal
communities (Scott and Russ 1987), reduced abundance
of herbivorous ®shes (Russ 1984a), and reduced diversity of overall ®sh fauna (Williams and Hatcher 1983).
Klumpp and Pulfrich (1989) con®rm that ®shes, as opposed to invertebrates, are the dominant herbivores on
the Great Barrier Reef. Nutrient enrichment experiments at One Tree Reef on Australia's Great Barrier
Reef did not exhibit expected increases in algal standing
stock due to herbivory (Hatcher and Larkum 1983).
More recently, McCook (1996) has demonstrated that
the long-observed cross-shelf gradient in macroalgal
standing stock, often presumed to result from waterquality gradients, is in fact largely attributable to
increased herbivory on the oshore reefs.
For the Indian Ocean region, reports on herbivore
assemblage structure are limited (Chabanet et al. 1995;
Jennings et al. 1996; Letourneur 1996a, 1996b). Extensive work on the behavior and feeding patterns within
the family Acanthuridae was completed by Robertson
et al. (1979), Robertson and Polunin (1981), and Robertson and Gaines (1986). Hay (1984) used herbivory
bioassays in the Seychelles to document relatively higher
herbivory pressure on shallow reef slopes in comparison
to adjacent reef ¯at and sand-plain habitats. Lastly,
extensive studies on herbivory and herbivore assemblages in over®shed and marine reserve areas in Kenya
have shown that intense ®shing has strong direct and
indirect impacts on herbivore assemblage structure,
herbivory intensity, and resulting benthic community
structure (McClanahan and Sha®r 1990 ; McClanahan
1994 ; McClanahan et al. 1994).
The Republic of Maldives is a string of coral reef
atolls o the southwest coast of India. Despite an ecoFig. 1 Map of sites surveyed
for herbivorous ®sh assemblage and Thalassia assays
(additional sites I7 and I8).
Alpha-numeric code indicates
habitat type and corresponds to site codes in other
tables and ®gures. FT Faro
reef top; F faro reef slope;
I reef slope inside atoll rim;
O reef slope outside atoll rim
nomy that is essentially completely dependent on marine
resources including ®sheries, the reef ®sh stocks are
among the least exploited as the artisanal ®sheries have
traditionally focused on pelagic species, especially tuna.
Thus, Maldives reef ®sh communities are relatively undisturbed and present a valuable opportunity to examine
herbivorous ®sh communities and herbivory processes in
a reef system with relatively little trophic disruption.
In this study, we sought to quantify herbivorous ®sh
assemblage structure across habitat types and relate
herbivore populations to rates of herbivory, estimated
by a bioassay technique, across habitat types on reefs in
Laamu Atoll, Republic of Maldives.
Methods
Study area
Laamu Atoll (2.0°N, 73.5°E) lies in the southern third of the atoll
chain comprising the Republic of Maldives (Fig. 1). The Laamu
Atoll lagoon reaches a depth of 73 m. The atoll rim has fringing
reefs on the lagoon side and the outer, oceanic side. Fringing reefs
on both sides have similar zonation with a shallow sandy lagoon,
reef ¯at, reef crest, and reef slope. The outside slope drops precipitously to about 30±50 m, slopes gently for about 0.5 km, and
then drops o to abyssal depths (Anderson et al. 1992). The inside
reef slopes gently to about 20 m depth and grades into a sandy
bottom. In the central portion of the lagoon, pillar reefs called
faros reach from the sandy lagoon ¯oor to within a few meters of
the surface. Zonation in faros was similar to the fringing reefs
except they do not have a sandy lagoon. Study sites were chosen for
both their representativeness of these habitats as well as proximity
to the Oceanographic Society's laboratory (near site I2, Fig. 1). All
surveys were conducted June±July 1997, which falls just after the
shift to the SW monsoon. The portion of the atoll where our study
sites were located receives high wave energy during this season.
Herbivorous ®sh assemblages
Twenty sites were surveyed for herbivorous ®sh density and assemblage structure (families Acanthuridae, Scaridae, and Siganidae) among four habitat types: faro reef ¯ats, faro reef slopes, and
reef slopes both inside and outside the atoll rim (Fig. 1). At each
site, eight 100-m2 transects (20´5 m, width by visual estimation)
were searched for all ®sh of the aforementioned families greater
31.0
(4.0)
24.8
(3.0)
22.6
(2.2)
33.0
(3.6)
25.4
(5.5)
21.2
(3.4)
35.9
(4.4)
26.9
(6.4)
22.3
(3.7)
32.9
(6.8)
18.6
(4.8)
13.9
(3.1)
10.1
(2.1)
8.8
(1.6)
21.6
(4.9)
15.5
(2.7)
21.6
(3.3)
25.6
(2.9)
22.3
(1.9)
Total
herbivores
25.3
(4.0)
0.8
(0.4)
0.4
(0.3)
0.9
(0.6)
0.3
(0.3)
0.3
(0.3)
0.6
(0.3)
0.4
(0.3)
1.0
(0.5)
0.3
(0.3)
2.9
(0.9)
±
0.2
(0.2)
±
±
±
0.3
(0.3)
0.1
(0.1)
0.1
(0.1)
±
Siganidae
(4 species)
0.3
(0.3)
7.6
(2.5)
2.9
(0.6)
3.0
(0.7)
3.9
(1.9)
11.0
(3.8)
9.9
(3.0)
19.6
(2.8)
9.0
(2.0)
6.6
(2.0)
15.3
(4.0)
10.0
(3.1)
7.3
(1.9)
3.4
(1.3)
2.5
(0.4)
9.4
(3.9)
0.8
(0.3)
1.5
(0.6)
3.0
(1.6)
5.4
(1.7)
Scaridae
(14 species)
2.6
(0.4)
22.6
(3.5)
21.5
(2.7)
18.7
(1.7)
28.9
(3.5)
14.1
(2.1)
10.8
(1.3)
15.9
(1.9)
16.9
(5.1)
15.4
(2.3)
14.7
(3.3)
8.6
(1.7)
6.4
(1.2)
6.4
(1.0)
6.2
(1.6)
12.2
(1.6)
14.5
(2.7)
20.0
(3.8)
22.5
(2.2)
16.9
(1.4)
22.4
(3.6)
1.2
(0.0)
1.2
(0.0)
0.9
(0.0)
1.4
(0.0)
7.7
(0.6)
7.0
(0.9)
6.0
(0.5)
5.4
(0.8)
6.8
(0.3)
5.4
(0.3)
8.1
(1.1)
8.5
(0.8)
16.5
(1.1)
9.2
(0.0)
7.0
(0.8)
11.4
(1.2)
7.1
(0.9)
9.7
(0.8)
8.1
(1.1)
FT4
FT3
FT2
FT1
F5
F4
F3
F2
F1
I6
I5
I4
I3
I2
I1
O5
O4
O3
Acanthuridae
(12 species)
Total herbivorous ®sh density was highest in the faro
reef ¯at habitat type and lowest on the inside atoll rim
habitat type (Table 1, Fig. 2). Acanthurids were most
8.9
(0.9)
Herbivorous ®sh assemblages
Depth (m)
Results
O2
Relative grazing intensity was compared among the same four
habitat types (faro reef ¯at, faro reef slope, and reef slopes inside
and outside the atoll rim) using a bioassay technique. Assays were
performed at two sites in each habitat type (eight sites in total).
Thirty-centimeter pieces of polypropylene rope were prepared by
placing three clean, 5-cm lengths of Thalassia seagrass blades securely between the twisted twines. At each site ten such ropes were
placed on the reef and left available for grazing for 91 (11) min
(SD). After retrieval, Thalassia blades were scored as follows:
1=not eaten, 2=<50% consumed, 3=51±90% consumed, and
4=completely consumed. These scores were treated as ranks and
the mean ranks for each rope (mean of three blades per rope) were
used as replicates to test for signi®cant dierences among sites by
non-parametric Kruskal-Wallis ANOVA followed by Dunn's
tests (pairwise post-hoc comparisons) to examine the similarity of
sites of the same habitat type.
At one inside atoll rim site (I2 on Fig. 1), the grazing preferences of herbivores were examined by presenting four common
macrophytes for consumption: Eucheuma cottonii, Thalassia sp.,
Padina sp., and Lobophora sp. Eucheuma cottonii is an exotic
species which is being cultivated in an experimental mariculture
facility in nearby lagoons, while the latter three species are all
naturally abundant in nearby habitats. The site was divided into
three depth zones: shallow reef ¯at (1±3 m), reef slope (10 m), and
knoll (15±20 m). The knoll habitat is a deeper coral mound consisting of plate and massive corals. In this assay, each rope contained one frond of each of the four macrophyte types, and 30
ropes were presented in each of the three habitats. The ropes were
collected after approximately 3 h and each plant piece scored in
the same manner as the Thalassia bioassay. Scores were used as
ranks in non-parametric Kruskal-Wallis ANOVAs with Dunn's
post-hoc comparisons to test for dierences in consumption between reef zones for each plant type.
O1
Herbivory processes
Site
than 5 cm total length. Fish were enumerated by species. Observers were trained to estimate transect width by placing construction ¯ags at a distance estimated to be 2.5 m from each side
of the length of a transect line. The actual distance was then
measured and biases made known to observers. This process was
repeated until observers could accurately estimate transect width.
Parrot®sh (Scaridae) in the Maldives are dichromatic, so initial
phase and terminal phases were also enumerated in order to determine if the separate phases show dierent distribution patterns.
A nested ANOVA was used to assess dierences in mean species density among habitat types and among sites nested in habitat
types (Zar 1984). Tukey tests were used to make pairwise comparisons for signi®cant factors. Data were log (x+1) transformed
due to heterogeneous variances. Total and family herbivore density were similarly tested. Multivariate analyses were performed
using MVSP software (Kovach Computing Services, Pentraeth,
Isle of Anglesey, Wales, UK). The percent similarity coecient was
used to examine the similarity of species density among the four
habitat types. Cluster analysis was performed using the group
average linkage method. Relationships between depth of survey
and species abundance were examined with a Pearson correlation
coecient, and signi®cance was judged using Bonferroni adjusted
probabilities (Zar 1984). Depth relationships were also investigated by creating histograms of the seven most abundant species,
including both parrot®sh phases, by depth in 3-m categories.
Table 1 Summary of mean density of herbivorous ®sh as (number of ®sh)á100 m±2 (1 SE) in Laamu Atoll, Republic of Maldives. Site codes are as described in Fig. 1 and indicate
habitat type of the site: O Reef slope outside atoll rim; I reef slope inside atoll rim; F faro reef slope; FT reef ¯at on faro tops
257
258
abundant among faro reef ¯at and outside atoll rim reef
slope sites, while scarids showed the opposite pattern.
Thirty herbivorous ®sh species were observed during this
study, with surgeon®sh (Acanthuridae) being repre-
Fig. 2 Herbivorous ®sh density, for three herbivore families and
total, sampled in visual transects among four reef habitat types
(n=4±5 sites within each habitat type)
Table 2 Signi®cant results of
nested ANOVA with habitats
and sites nested within habitats
as ®xed factors (ns non-signi®cant; * p<0.05, ** p<0.01, and
*** p<0.001). Signi®cant
dierences show the results of
pairwise comparison testing for
eect of the main factor habitat
type. Habitat types examined
are the reef ¯at on top of faros
(farotop), reef slope in faros
(faro), inside atoll rim (inside),
and outside atoll rim (outside).
IP Initial phase; TP terminal
phase
sented by 12 species, parrot®shes (Scaridae) by 14 species, and rabbit®sh (Siganidae) by 4 species (Appendix 1,
see electronic supplementary material). Eleven species
showed signi®cant density dierences among habitat
types (Table 2). Faro reef ¯ats were characterized by
higher than average abundances of Acanthurus lineatus,
A. luecosternon, and A. nigrofuscus. Initial phase (IP)
Cetoscarus bicolor, Naso literatus, and IP Scarus sordidus were most abundant on faro reef slopes. The reef
slope inside the atoll rim was characterized by high
abundance of IP Hipposcarus harid. The surgeon®sh
A. luecosternon, Ctenochaetus strigosus, and Zebrosoma
desjardini were most abundant on reef slopes outside the
atoll rim. Clustering revealed distinct grouping by habitat type (Fig. 3). Outside atoll rim reef sites were 74.5%
similar, faros 61.1%, and inside atoll rim reef sites
51.0%. Three of the four faro reef ¯at sites were 77.6%
similar, with the fourth site grouping with outside atoll
rim reef sites.
Nine of the 45 correlations between depth and species
[including both initial (IP) and terminal phase (TP)
parrot®sh] were signi®cant and all were negative. How-
Fig. 3 Cluster diagram showing relationship of herbivore assemblage and habitat types. Site codes correspond to Fig. 1 and
Table 1. Habitat types that clustered together are represented as a
group and individual sites that did not cluster with their habitat
type as their site code. For example, all outside atoll rim reef slopes
clustered together and were 75% similar as measured by the
percent similarity index
Species
Habitat
Site
Signi®cant dierences
Acanthurus lineatus
A. luecosternon
A. nigracauda
A. nigrofuscus
Ctenochaetus striatus
C. strigosus
Naso literatus
Total Acanthuridae
Cetoscarus bicolor (IP)
Hipposcarus harid (IP)
Scarus frenatus (TP)
Scarus ghobban (IP)
Total Scaridae
***
***
*
**
***
***
***
***
***
***
*
*
***
ns
*
***
***
***
***
ns
***
**
**
ns
ns
***
Grand total
***
***
Farotop > faro = outside = inside
Outside = farotop > faro > inside
Inside > outside
Farotop > faro = outside = inside
Farotop > faro > inside > outside
Outside > farotop = inside = faro
Faro > inside = outside = farotop
Farotop = outside > faro > inside
Faro > farotop = outside = inside
Inside > faro = outside = farotop
Faro > farotop, farotop > outside
Inside > farotop
Faro > farotop = outside, faro = inside,
inside = farotop, inside > outside
Farotop = faro = outside > inside
259
ever, after adjusting for the high number of correlations
calculated, only Acanthurus lineatus (r=±0.37, p<0.01),
A. luecosternon (r=±0.32, p<0.05), and Ctenochaetus
striatus (r=±0.49, p<0.001) remained signi®cant. Figure 4 shows that A. lineatus was rarely observed in water
greater than 3 m deep, while A. luecosternon density
decreased gradually with increasing depth. The two most
abundant Ctenochaetus species, striatus and strigosus,
appear to have opposite distributions related to depth.
Ctenochaetus striatus was most abundant in shallow
water, <3 m depth, with a secondary rise in abundance
after 12 m depth. The opposite pattern was observed for
C. strigosus; the species showed increasing abundance to
12 m depth, then a decrease thereafter. The remaining
®ve species all showed peak densities at 6 m. Thereafter,
Scarus niger and TP S. sordidus decreased in density
Fig. 4 Mean abundance (number of ®sh per transect) +1 SE
of the seven most abundant
herbivorous ®sh species in 3m-depth strata. Data are pooled
for all habitat types and sites
(n=160 transects). Initial phase
(IP) and terminal phase (TP)
®sh are presented separately for
the two scarid species where
they are readily discernible
until secondary peaks at 15 or 18 m depth. IP S. sordidus
showed no consistent pattern with depth, while Zebrasoma scopas appeared to be equally abundant at depths
greater than 3 m.
Herbivory processes
There was signi®cant variation in the rates of herbivory
among sites and habitat types in standardized Thalassia
assays (Fig. 5A). Relative grazing rates were highest at
the inside atoll rim reef slopes and lowest in areas subjected to heavy waves and surge (outside the atoll rim
and faro reef ¯ats). The two inside sites were statistically
similar to each other (Dunn's test p>0.05) as were the
two outside sites. However, the two faros sampled were
260
(p=0.121). The herbivorous ®sh assemblage at the reef
slope and knoll sites (sites I2 and I3, Table 1) appears
quite similar.
Discussion
Herbivorous ®sh assemblages
Fig. 5 Relative herbivory pressure at Laamu Atoll. Bars represent
mean grazing rank score (+1 SE, see text). A Comparison among
two sites of each of the four habitat types as measured by the
Thalassia assay (n=10 ropes per site, three blades per rope).
Standard error for site 3 was zero since all replicates had grazing
rank =3. Bars with the same letter do not dier signi®cantly
(p>0.05) according to Dunn's pairwise post hoc comparisons. B
Comparison of herbivore preference among four plant types in
three depth zones at site I2. P Values from Kruskal-Wallis nonparametric ANOVA; n=29±30 for each plant type
substantially dierent from each other and obscured any
similarity of relative herbivory by habitat types (faro
slope versus faro ¯at).
The choice assay comparing herbivore preference
among plant types in three depth zones (site I2) indicated signi®cant selectivity of grazers (Fig. 5B), with the
exotic Eucheuma cottonii experiencing the highest rates
of consumption, Thalassia intermediate, and Lobophora
and Padina experiencing similarly low consumption.
Three of the four plant types displayed signi®cant variation in susceptibility to herbivores among depth zones
(Fig. 5B, Kruskal-Wallis non-parametric ANOVAs).
Three species suered highest consumption in the middepth slope habitat, the exception being Lobophora sp.,
which had the lowest proportion of blades consumed in
the slope habitat compared to the other two habitats.
Overall herbivory rates among the three depths at this
site (four plant types pooled) did not dier signi®cantly
This article reports for the ®rst time on the structure of
herbivorous ®sh assemblages among coral reef habitat
types in the Republic of Maldives. We show that certain species of ®sh were most abundant on a particular
coral reef type. In this study, three types of coral reef
slopes were examined as well as one type of reef ¯at.
Herbivorous ®sh assemblages were more similar among
sites within a particular coral reef type than among
types; our study sites clustered into four groups which
corresponded to the four coral reef types studied. Faro
and inside atoll rim reef slopes were most similar to
each other with respect to herbivorous ®sh composition
and quite dissimilar to outside atoll rim reef slopes and
faro reef ¯ats. Clustering of sites among habitat types
appeared to be mainly due to the dierential distribution of acanthurids and scarids, the former being more
abundant among faro reef ¯at and outside atoll rim
reef slope sites and the latter more abundant among
faro and inside atoll rim reef slopes. There are a
number of possible explanations for this result. These
include dierences in algal preferences among families
or species (Choat 1990), species interactions including
territoriality (Robertson and Gaines 1986) and
schooling patterns (Choat and Bellwood 1985), and
dierential habitat use (Jennings et al. 1996). The
present study did not collect information on the
abundance of preferred food items at study sites.
However, the potential role of major dierences among
habitats such as depth and environmental gradients can
be examined for their utility in explaining observed ®sh
abundance patterns.
Depth distributions indicate that depth signi®cantly
in¯uenced the abundance of the nine most abundant
species. Several species were most abundant in depths
less than 3 m, while others clearly showed peaks of
abundance at 6 m. However, depth alone does not explain the similarity in assemblage structure among outer
atoll rim reef slopes and faro reef ¯ats as opposed to faro
and inside atoll rim reef slopes. For example, Acanthurus
luecosternon was signi®cantly more abundant on outer
atoll rim reef slopes and faro reef ¯ats than faro and
inner atoll rim reef slopes (Appendix 1; see electronic
supplementary material). Yet, the mean depth of sites
(1 SE) outside the atoll rim was 9.0 (0.7) and in faro
reef ¯ats 1.2 (0.1). Also, there was no signi®cant dierence in the average depth of sites in the three reef slope
habitat types (Tukey HSD multiple comparison test,
p>0.05). Similarly, Ctenochaetus strigosus were more
abundant on outer rather than inner atoll rim reef slopes
(Appendix 1; see electronic supplementary material).
261
Yet there is essentially no dierence in the average depth
of these sites (9.0 versus 9.1 m depth).
While it is not possible to examine the abundance of
species relative to the distribution of their preferred prey
items, we can examine some of the general characteristics
of these habitats which might in¯uence the observed
distribution patterns. Clearly, faro reef ¯ats and outer
atoll rim reef slopes share very few characteristics.
However, one important feature they both share is that
they are subjected to intense wave action, whereas the
other two reef slope types are generally more protected.
Faro reef tops are shallow, averaging only 1.2 m depth.
During our sampling season (the SW monsoon) these
sites are subjected to heavy waves. Similarly, outer atoll
rim reef slopes bear the brunt of oceanic waves travelling
across the Indian Ocean. At times, surge can be felt
down to 20 m (R. Sluka, personal observation). This
result is similar to data presented by Williams (1982)
who showed that changes in the abundance and species
composition of herbivorous ®sh assemblages on the
Great Barrier Reef around Raine Island were related to
the incident wave energy. Both inner atoll rim and faro
reef slopes were similar in the structure and exposure to
wave energy. These reef slopes appeared to be structurally more complex than outer atoll rim reef slopes, as
evidenced by the height of corals relative to the slope and
the amount of massive coral growth (R. Sluka, personal
observation). Outer atoll rim reef slopes tended to be
steep slopes with mostly plate coral growth forms and a
greater abundance of the calcareous algae Halimeda spp.
In the current study, Acanthurus lineatus was mostly
restricted to faro reef ¯ats. This result is similar to Russ's
(1984b) study on zonation patterns in the Great Barrier
Reef. He studied ®ve coral reef zones from the back reef
to reef slope. In his study, Acanthurus lineatus was only
found on the reef crest. This species was not found on
the reef ¯ats in his study. However, reef ¯ats in Russ's
study diered from the faro reef ¯ats in this study in
their wave exposure. Russ (1984a) describes his reef ¯at
study sites as situated 75±150 m behind the windward
reef crest. This would indicate that the waves broke on
the crest and were substantially reduced by the time they
reached the reef ¯at study area. In contrast, faro reef ¯at
sites in the Maldives were situated within the circular
faro reefs and were 20±50 m in diameter. During the SW
monsoon (May±October), these faro reef ¯ats experience
considerable wave energy. Any wave action will produce
surge on the reef ¯ats, especially at low tide when the
depth at these sites is reduced below 1 m. A similar
pattern was found for Acanthurus nigrofuscus and Ctenochaetus striatus. In both this study and Russ's (1984b),
these species were more abundant in coral reef zones
subjected to greater wave exposure. Russ (1984b) also
noted, similar to this study, that Acanthurus nigrofuscus
was more abundant in the shallower zones. This study
and that of Russ (1984b) also found that Scarus niger
was more abundant in deeper than shallower zones.
The territorial microherbivores Ctenochaetus striatus
and C. strigosus are known to mutually exclude each
other from their respective territories, yet have broad
overlap in habitat use (Robertson and Gaines 1986).
However, in the Maldives, there appears to be a greater
segregation by habitat and depth. C. striatus was least
abundant on outer atoll rim reef slopes, while C. strigosus was most abundant in this habitat type. Figure 4
shows that these species were most abundant at dierent
depths. The former species was most abundant in shallow depths (<3 m) with a secondary peak at 18 m.
C. strigosus, however, had a unimodal distribution almost opposite that of C. striatus; abundance peaked at
12 m depth. The reasons behind this greater segregation
in the Maldives versus Aldabra, the Seychelles, are
unknown, but one cause might be that these species
competed more strongly at the Maldivian study sites.
There were very few dierences in habitat use among
initial and terminal phases of a particular parrot®sh
species. Of the 14 parrot®sh species, only four exhibited
dierential habitat use. There did not appear to be any
pattern among phases or species.
Herbivory processes
Signi®cant variation in relative herbivory pressure
among reef zones as measured by the Thalassia bioassay
and the choice assay is consistent with the results of Hay
(1984) at two sites in the Seychelles. His study found
highest herbivory pressure in reef slope habitats as
compared with reef ¯ats and deep sand plains, a pattern
similar to that on Caribbean reefs. The current study
also showed highest consumption of three out of four
plant types in reef slope zones, compared with adjacent
depth zones (Fig. 5B).
Among habitat types, low Thalassia consumption
pressure was observed at the outside atoll reef slope
habitat type and at one of the two faro sites (both faro
slope and faro ¯at habitat types). High wave energy may
explain the low consumption rate in the outside reef
slope habitat type. The substantial dierence in herbivory pressure between the two faro sites sampled may
result from divergent ecological history. Many faros in
Laamu Atoll, especially those closest to the atoll villages,
were previously mined for building material (Sluka and
Miller 1998). The speci®c history of the two faros sampled is not documented, however.
Interestingly, the highest relative consumption in the
Thalassia assay was at the inside atoll rim habitat type,
where total herbivorous ®sh density was lower than the
other sampled habitats. One factor that may result in
discrepancies between herbivore density and consumption rate has to do with the sizes of the individual ®sh.
Harmelin-Vivien (1984) reports similar densities of
scarids and acanthurids in lagoonal and outer atoll reefs
at Tikehau Atoll in French Polynesia. However, because
large adults were more prevalent on the outer reefs,
and juveniles more abundant in lagoonal habitats, the
areal biomass of herbivorous ®shes was greater on the
outer slope than the lagoonal reefs. Acanthurids are also
262
reported as the predominant herbivorous ®shes on the
outer reef slopes.
Lastly, it is known that Thalassia assays primarily
indicate consumption by Scaridae (McClanahan et al.
1994). In fact, density of Scaridae across habitat types
shows a more congruent pattern with consumption in the
Thalassia assay than does total herbivorous ®sh density
(Figs. 2 and 5A). Acanthurid density was higher than
scarid density in each habitat type sampled in the current
Laamu Atoll study, contrasting with herbivorous ®sh
assemblages reported in the Caribbean where scarids
often dominate acanthurids in both density and diversity
(Schmitt 1997 ; Schmitt et al. 2001). Hence, Thalassia
assays may be a less useful indicator of overall herbivory
processes in the Indian Ocean than in the Caribbean.
Acknowledgements This study was made possible by a grant from
the National Geographic Society Committee on Research and
Exploration. Logistical support was provided by the Oceanographic Society of the Maldives. Field assistance by Yoosuf Nishar
and Abdullah Hakeemu is greatly appreciated.
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