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Disturbance, Habitat Structure, and the Dynamics of a Coral-Reef Fish
Community
Craig Syms; Geoffrey P. Jones
Ecology, Vol. 81, No. 10. (Oct., 2000), pp. 2714-2729.
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Ecology, 81(10), 2000, pp. 2714-2729
O 2000 by the Ecological Society of Amerlca
DISTURBANCE, HABITAT STRUCTURE, AND THE DYNAMICS OF A CORAL-REEF FISH COMMUNITY CRAIGSYMS'AND GEOFFREYP. JONES
Department of Marine Biology, James Cook University, Townsville, Queensland 481 1, Australia
Abstract. Coral reef fishes occupy habitats that are patchy and subject to frequent
natural disturbances. Although different types of disturbance are likely to generate different
community responses, the relationship between different disturbance agents and their effects
on reef fish communities has not been examined experimentally. We studied a set of natural
patch reefs, dominated by a diverse array of soft and hard coral cover, at Lizard Island on
the Great Barrier Reef (northeastern Australia). The fish assemblages on the reefs were
sampled over 4 mo to establish baseline values and then experimentally disturbed. Two
types of disturbance were carried out in a factorial combination: pulsed mortality by removing all fish from reefs and pulsed habitat disturbance. Habitat disturbance was applied
at two levels: Level 1 consisted only of damaging all live hard corals with a hammer; Level
2 consisted of damaging all live hard corals, and in addition, using a hammer to reduce
the height and complexity of the reef matrix. We then monitored the experiment for a further
19 mo, including two recruitment seasons.
unmanipula&d control assemblages persisted through time, and despite large changes
in total abundance. species comvosition remained consistent relative to disturbed treatments.
Assemblages disturced by fishAremovalwere resilient, with recolonization from both immigration and larval settlement effectively removing differences between removal treatments and controls 3 mo after manipulation. Habitat disturbance alone generated differences
between experimental and control assemblages, which persisted for the duration of the
experiment. The more extreme level of habitat disturbance generated more extreme changes
in fish assemblages when no pulsed mortality occurred. Habitat disturbance in combination
with pulsed mortality generated similar community responses as the habitat disturbance
treatment alone. However, fish removal had the effect of eliminating the difference between
fish assemblages on reefs subjected to different levels of habitat disturbance. Community
response to habitat disturbance was driven by species-specific patterns of reduced abundance
of species associated with live coral in combination with increased numbers of those associated with rubble. Declines in the abundance of coral associates on damaged reefs were
abrupt, with no recovery observed for the duration of the experiment. In contrast, increases
in the abundance of rubble associates were more ephemeral, in that initial high levels of
recruitment and immigration were followed by a high rate of loss. Habitat disturbance also
generated reefs that typically supported lower fish abundance, fewer species, and increased
evenness relative to controls.
Our results support a model of patch-reef fish assemblages organized by a combination
of deterministic factors (such as habitat structure) and stochastic processes (such as recruitment). These disparate mechanisms operate in concert to generate reasonably consistent
patterns of community structure. Habitat structure appears to mediate much of the apparent
determinism and is likely to operate both as a reflection of species-specific habitat preferences and by modifying interactions among fish species. Consequently, disturbance plays
a substantial role in structuring communities of coral-reef fishes by modifying both spatial
and temporal heterogeneity.
Key words: community structure; coral reef$sh; disturbance; fish removal; Great Barrier Reej
Australia; habitat structure; patch reefs.
INTRODUCTION
Disturbance plays a central role in the dynamics of
a wide variety of ecological communities (Dayton and
Manuscript received 29 June 1998; revised 3 September 1999;
accepted 6 October 1999.
I Present address: Biology Department, Earth and Marine
Sciences Building, university of california, santa c r u z , ca1ifornia 95064 USA. E-mail: [email protected]
Hessler 1972, Paine and Levin 1981, Sousa 1984, Pickett and White 1985, Krummell et al. 1987, Karlson and
Hurd 1993). The predicted effects of disturbance depend not only on the magnitude and type of disturbance, but also on the mechanism by which the disturbance agent operates. For example, extreme disturbance can reduce diversity and alter community structure by eliminating species (Petraitis et al. 1989, Pickett
et al. 1989). In contrast, moderate levels of disturbance
October 2000
DISTURBANCE EFFECTS ON REEF FISH
may promote local diversity by reducing the abundance
of competitively dominant species and allowing inferior competitors to persist (Connell 1978, Petraitis et
al. 1989). Different disturbance agents may exert different types of effects on species. Disturbances that
remove key resources in the system (e.g., trees, macroalgae, corals), which provide biogenic habitat for
other suites of smaller organisms (e.g., insects, amphipods, fishes), may have very different consequences
than mortality of the smaller organisms alone. The relative importance of different types of disturbances in
systems where the disturbance may act directly on the
focal community or indirectly via habitat effects has
received little attention (Jones and Syms 1998).
The type of response that disturbance generates in a
community is to a large degree contingent on how it
affects the demography of individual species and disrupts interactions among species (Petraitis et al. 1989).
Disturbance may exert density-independent effects by
introducing increased variability into a system, thus
reducing the strength of density-dependent interactions
(Huston 1979, Strong 1983). Disturbance may also alter density-dependent factors such as per capita death
or birth rates (e.g., by promoting selective mortality,
Connell 1978) and thus might be expected to generate
density-dependent effects on other species in the system. Spatial heterogeneity may also be generated by
disturbance, which may operate to reset successional
stages of patches within a mosaic (Clark 1991). Therefore, in order to develop a model of disturbance effects
on a particular community, it is necessary to compare
and contrast the species-specific responses to the disturbance agent.
Disturbance-induced heterogeneity has the effect of
fragmenting populations and communities into patches.
Two major consequences of this fragmentation are the
introduction of extra levels of variability into the system and an increase in average between-patch differences in dynamics. Consequently, both within- and between-patch dynamics are central components of models of community mosaics and are an important part of
deriving a model of large-scale community dynamics
(Chesson 1997). The patch may also be the spatiotemporal unit within which key density-dependent processes operate to regulate population numbers (Hassell
et al. 1987). Consequently, understanding the relationship between dynamics of different patches as a function of disturbance is a central requirement for studying
fragmented communities.
Coral-reef fish communities provide a tractable system in which to examine the consequences of different
types of disturbance in "open" patchy systems. Coral
reefs are inherently patchy at all stages of their development. They are also subject to frequent, often catastrophic disturbances, such as cyclones and crown-ofthorns starfish damage, which may induce patchiness
in the habitat and their associated fish assemblages
(Connell 1978, Bouchon-Navaro et al. 1985, Harmelin-
2715
Vivien and Laboute 1986, Dollar and Tribble 1993,
Hughes 1994). However, disturbance processes have
been largely overlooked in the development of reeffish community theory (but see Chesson and Huntly
1997). Instead, empirical studies have focused on the
degree of predictability of reef fish assemblages and
the roles of competition and recruitment in changing
levels of predictability. The early preconception of
these communities as tightly organized, predictable
units (e.g., Smith and Tyler 1972, Gladfelter and Gladfelter 1978, Smith 1978) was superseded in the 1970s
by the view that coral-reef fish assemblages were nonequilibria1 in nature. An initial formulation of this idea
held that the community was composed of competitors
of equal ability vying for space on the reef and replenished at random from the plankton (the "lottery"
hypothesis; Sale 1977). With the realization that space
was not necessarily limiting, the lottery hypothesis was
itself superseded in the 1980s. The new model emphasized the increased role of recruitment variability,
combined with an absence of competitive and other
density-dependent processes in limiting the overall size
of the community (the "recruitment limitation" hypothesis; Doherty 1983, Victor 1983, 1986). It is now
clear that both density-dependent and density-independent processes are likely to regulate community structure. Appeals for pluralism on both empirical (Jones
1990, 1991, Forrester 1995, Hixon and Carr 1997, Ault
and Johnson 1998) and theoretical (Chesson 1985, Hixon 1991, 1998, Caley et al. 1996) grounds highlight
the need to examine previously untested factors.
Given the potential for disturbance to modify density-dependent interactions (Chesson and Huntly
1997), and the frequency of natural disturbance agents
in coral reef environments, there is a need for more
empirical examination of disturbance in coral-reef fish
communities (Jones and Syms 1998). Disturbance experiments, in which perturbations were applied by removing reef fish and observing recolonization, have
been conducted to measure the degree of determinism
of assemblages (e.g., Sale and Dybdahl 1975, 1978,
Sale 1980). These studies have generally identified a
large degree of unpredictability in community structure. Natural analogs of disturbances resulting in direct
mortality, however, have been rarely recorded and consequently may play an infrequent role in the dynamics
of the community. However, hypothermic conditions
have caused fish kills in the Florida Keys (Bohnsack
1983), and catastrophic storms have reduced fish numbers in Hawaii (Walsh 1983) and on the Great Barrier
Reef (Lassig 1983).
Disturbance of key habitat components has received
little attention in coral-reef fish communities despite
its potential importance and frequent natural occurrence (Lewis 1997a, 1998, Jones and Syms 1998, Syms
1998). Experimental investigations are few, possibly
because fish communities are often only weakly correlated with habitat variables at scales that habitat can
2716
CRAIG SYMS AND GEOFFREY P. JONES
be manipulated (e.g., Sale et al. 1994, Ault and Johnson
1998). In contrast with tropical systems, experimental
habitat disturbances have been widely and successfully
applied to temperate reef-fish assemblages (Choat and
Ayling 1987, Bodkin 1988, Jones 1988a, 1992, Carr
1989, 1991, DeMartini and Roberts 1990, Holbrook et
al. 1990, Syms and Jones 1999). These studies have
generally demonstrated that habitat disturbance may
exert large and locally persistent effects on the dynamics of fish communities. However, the relative importance of both types of disturbance and their effect on
coral-reef fish assemblages has not been examined.
It is likely that habitat variables play a central role
in determining the structure of reef fish assemblages.
Species-specific habitat choices as adults and at settlement (Kaufman et al. 1992) determine the degree of
spatial overlap between members of the community.
Habitat structure is also likely to mediate key events
operating at the scale of individuals by providing shelter from predation (Hixon and Beets 1993) and modifying competitive interactions and survivorship (Jones
1988b). However, empirical studies have been divided
about whether fish are strongly (e.g., Bell and Galzin
1984, Bell et al. 1985, Findley and Findley 1985, Bouchon-Navaro and Bouchon 1989, Hart et al. 1996) or
weakly (e.g., Roberts et al. 1988, Fowler 1990, Booth
and Beretta 1994, Cox 1994, Green 1996) associated
with habitat variables. Unfortunately many of these
studies are difficult to compare and evaluate, due to
confounding factors and the different ranges of habitat
conditions considered (Jones and Syms 1998). In order
to gauge the effects of habitat disturbance on fish assemblages, a range of disturbance levels are required
to generate effects that can be measured above the baseline level of within-patch variability.
In this study, we experimentally examined the effects
of fish removal and habitat disturbance on the structure
of fish assemblages occupying small coral patch reefs
at Lizard Island (Great Barrier Reef, Australia). To do
this, we administered a factorial combination of complete fish removal with two levels of habitat disturbance
(Level 1: the breaking-up of all hard corals on the patch
reef; Level 2: the breaking-up of hard corals coupled
with reducing the physical structure of the reef). This
approach allowed us to test the hypothesis that habitat
structure mediates the local organization of reef fish
assemblages. If this hypothesis was true, then three
outcomes of this experiment could be predicted: (1)
Fish removal alone should result in recolonization of
species to form an assemblage that resembled the control reefs (Fig. 1A). (2) Habitat disturbance alone
should result in fish assemblages that differ from those
of controls (Fig. 1B). (3) The combined effect of fish
removal and habitat disturbance should, following recolonization, result in assemblages which do not differ
from those of habitat disturbance alone (Fig. 1C).
Ecology, Vol. 81, No. 10
Control community
,. ***-
I
I
#
I
0
I
I
I
'
Fish removal
'
I
I
I
*-----
t
#
I I
11
#
4
Control community
Level 1 habitat disturbance
Level 2 habitat disturbance
\
1
a
I
I
**-
Habitat disturbance onlv
Habitat disturbance and fish removal
*
'
I /
Time
FIG. 1. Predicted responses of fish community structure
to different disturbances. The y-axis represents a multivariate
measure of community structure; the arrows indicate the time
at which the disturbance is carried out. (A) Removal of all
fish alone should result in recolonization to a community
structure that is similar to that of controls. (B) Habitat disturbance alone should generate persistent differences in community structure relative to controls. The degree of difference
should be related to the extremity of the disturbance. (C)
Habitat disturbance in combination with fish removal should
eventually result in a community that is the same as that
following habitat disturbance alone.
This study was carried out over 24 mo (July 1993June 1995) at Lizard Island (14'40' S, 14S028' E) on
the northern Great Barrier Reef, Australia. The study
October 2000
Control
DISTURBANCE EFFECTS ON REEF FISH
Habitat disturbance
Level 1
Level 2
FIG.2. Schematic representation of the experimental design. Level 1 habitat disturbance involved breaking all hard
corals, whereas Level 2 disturbance involved breaking hard
corals and further reducing the height and complexity of the
reef.
area was a 200 X 300 m field of patch reefs ranging
in size from 0.25 m2 to > I 0 0 m2 at 5-7 m depth on
the southwestern side of the island. A subset of 48 patch
reefs of similar size and coral composition, interspersed
among numerous other reefs, was selected for the experiment. Reefs were between 2 and 3 m long, 0.751 m wide, and generally < 1 m high. The spacing between reefs was variable, but experimental reefs were
on average -10 m from other patch reefs. The proximity of reefs in this system was such that movement
of more mobile fish species between reefs was likely,
so they cannot be considered as true isolates (cf. Sale
1980).
Experimental design
Two forms of disturbance were applied to the reefs
in a factorial design, with eight replicates per treatment.
Fish removal was carried out by removing fish from
half of the reefs using the anaesthetic Quinaldine (dissolved in alcohol and seawater) and hand-nets (Fig. 2).
Because the fish occasionally fell into crevices in the
reef matrix during anaesthetizing, we visited the reef
the following day and removed any fish still present.
Considering baseline fish counts immediately before
manipulation, the clearance was effective. Habitat disturbance was applied at two levels (Fig. 2). The first
level entailed the breaking-up of most of the hard corals
with a hammer; the second level was achieved by both
breaking-up the hard corals and reducing the height
and complexity of the reef matrix itself by additional
bludgeoning. All rubble resulting from the manipulation was left in place. Control reefs were not altered.
Fish were visually censused on 10 occasions-three
before manipulation and seven afterwards-over
a 2yr period. Each sample was a compilation of between
two and three repeated censuses, approximately following the procedure of Sale and Douglas (1981). Dur-
2717
ing each census, recently settled recruits were distinguished on the basis of size and coloration from the
established resident population of each species.
The reefs were measured and coral cover quantified
at three time intervals: before manipulation, 3 mo after,
and 12 mo after manipulation. Reef height was measured as the maximum height above the sand substratum. Coral cover was measured from a 30 cm wide
videotape-transect running over the top and around the
side of the reef. Twenty regularly spaced frames were
selected from the videotape, and the benthic cover under five random point intersects were recorded from
each frame to give a total of 100 point intersects per
reef. Only coral growth forms were recorded, as the
video did not allow resolution to species level.
Analysis
Predisturbance ordinations of benthic cover and fish
assemblages using principal components analysis indicated there were no preexisting compositional or spatial patterns in either the fish assemblages or coral cover
which could confound results (Dutilleul 1993). However, as a precaution against spatial confounding, the
reefs were grouped a priori into eight spatial blocks
oriented along the shoreline, and one replicate from
within these blocks was assigned randomly to each
treatment.
To assess preexisting relationships between fish assemblages and benthic cover, we used Mantel's test.
The fish data were root-root (xo29 transformed and
converted to a similarity matrix using the Manhattan
or Czekanowski proportional similarity index (Schoener 1968). Benthic cover data were square-root transformed (xo5)and converted to a similarity matrix using
the same index. A plot of fish vs. benthic similarities
did not reveal any nonlinearity that would affect the
Mantel's test. One thousand randomizations generated
the statistical test to the 0.001 level.
The experimental design contained three fixed factors-fish
removal (Removal), habitat disturbance
(Habitat) and time (Time)-and consequently the appropriate tests of treatment effects were the two and
three-way interactions (i.e., the trajectory of each manipulated factor over time) and not the simple effects.
As the data were repeated measures over time, we also
included reef (Reef) as a blocking factor to accommodate within-reef temporal structure. This split-plot
approach (SAS 1991) is an approximate test but provides a useful statistical guide. The model can be specified as (excluding mean and error term):
Variable, . . . Variable,
= Removal
Habitat + Removal X Habitat
+ Reef(Remova1 X Habitat) Time
+ Removal X Time + Habitat X Time
+ Removal X Habitat X Time
+
+
where Removal, Habitat and Removal X Habitat were
CRAIG SYMS AND GEOFFREY P. JONES
A) Undisturbed
60 1
-
1
1
60 lB) Habitat disturbance Level 1
1
B
& 40
0
.s 20
1 FIG. 3. Benthic cover of the major substratum categories on experimental reefs, before. 3
mo after, and 12 m o after two levels of habitat
disturbance. Total hard coral cover is highlighted in black.
e
I
Ecology, Vol. 81, No. 10
0
60 C) Habitat disturbance Level 2
40
20
0
Before
3 mo
Time after disturbance 12 mo tested over the blocking factor Reef(Remova1 X Habitat), and all other terms tested over the error,
We could not carry out a full multivariate analysis
of variance (MANOVA) of the fish data due to there
not being enough degrees of freedom (i.e., there were
too many fish species relative to the number of reefs
and levels of each factor). Consequently, we ran a principal components analysis on the covariance matrix of
the (x025)-transformedfish data and analyzed the first
20 principal components (which summarized 77.8% of
all the variation in the data set) with MANOVA, using
Pillai's trace as our test statistic. After MANOVA, we
developed a graphical presentation using canonical discriminant analysis (CDA) of the xoZ5-transformedfish
data using the three-way classification of Removal X
Habitat X Time as the hypothesis matrix.
In addition to the multivariate community analysis,
we also calculated species richness and evenness. Richness was quantified simply as the number of species
present on the reef. Evenness was calculated using the
E,,,, index (Smith and Wilson 1996):
2
E,,, = 1 - -arctan
7r
[r, (
ln(x,) -
,I,
RESULTS
Effectiveness of manipulation
The numbers of individuals removed from fish-removal reefs were comparable with baseline abundances, which indicated that the manipulation was effective.
In the first month after disturbance treatments, hard
coral cover had been reduced on the habitat-disturbance
reefs from 20-30% to < l o % (Fig. 3). The hard corals
that remained were generally encrusting favids-most
branching coral forms had been destroyed. Habitat-disturbance Level 2 also caused a 15% decrease in soft
coral cover, which persisted for most of the experiment.
None of the habitat-disturbed reefs regained their baseline coral compositions over the course of the experiment. During the experiment, control and Level 1 habitat disturbance reefs remained the same height, while
Level 2 habitat disturbance reduced the reef height by
5-7 cm.
Temporal patterns in community structure
TIs]
ln(x,)lS
which ranges from 0 (minimum evenness) to 1 (maximum evenness) and is insensitive to species richness.
Recruitment data were analyzed by combining recruit numbers for each reef across all censuses, transforming by XO.?~,
and analyzing the two-way factorial
MANOVA of Removal crossed with Habitat disturbance. Canonical discriminant analysis (CDA) of the
transformed data using the two-way classification
of Removal X Habitat provided graphical data presentation.
Both fish removal and habitat disturbance exerted
significant effects (Removal X Time, P = 0.0133; Habitat X Time, P = 0.0001; Table 1). No temporal interactions between the fish removal and habitat disturbance treatments (Removal X Habitat X Time, P =
0.2028) were apparent (Table I), which indicated that
the two disturbance forms had simple additive effects.
Two major community trends (changes in species composition and total abundance of adult fish) were evident
and covaried with the experimental factors. Species
composition accounted for the greatest portion of variation in community structure (canonical discriminant
1 = 37.4%). Compositional changes were driven by
DISTURBANCE EFFECTS ON REEF FISH
October 2000
2719
TABLE1. Multivariate analysis of variance of the first 20 bers of coral-associated species (e.g., Pomacentrus
principal components of the covariance matrix of the noZ5transformed data using a split-plot approximation model to moluccensis, Dascyllus reticulatus, D. aruanus, Gobiodon spp., Paragobiodon spp.), and a corresponding
incorporate repeated measures.
Source
Removal
Habitat
Removal X Habitat
Reef(Remova1 X Habitat)
Time
Removal X Time
Habitat X Time
Removal X Habitat X Time
Pillai's
trace
df
P
0.4475
20, 24
0.5210
1.3042 40, 50
0.0023
0.9292
40. 50
0.3894
6.6827 860, 7720 0.0001
2.5367 180, 3375 0.0001
0.5653 180, 3375 0.0133
1.5300 360, 6912 0.0001
0.9444 360, 6912 0.2028
Notes: The Removal treatment entailed a pulse removal of
all fish from the patch reef; the Habitat treatment involved
two levels of habitat destruction. Reef serves as the blocking
term.
different relative abundance of particular species. The
damselfishes Pomacentrus moluccensis, Dascyllus reticulatus, D. aruanus, Amblyglyphidodon curacao, and
P. nagasakiensis, gobies of the genera Gobiodon and
Paragobiodon, and the wrasse Halichoeres melanurus
were associated with positive loadings on the first canonical axis, whereas Parapercis spp., the damselfishes
Dischistodus perspicillatus, Pomacentrus coelestis,
Chrysiptera rollandi, and C. jlavipinnis, the wrasse
Halichoeres trimaculatus, and the goby Amblygobius
phalaena were all associated with negative loadings on
this axis (Table 2). Total abundance of adult fish accounted for the next greatest portion of the explainable
variation (canonical discriminant 2 = 9.2%) and corresponded with temporal changes both within and between experimental treatments.
One month following manipulation (December
1993), the community composition on reefs from which
fish had been removed was distinct from controls (Fig.
4 A ) , although no significant differences in total adult
abundance were apparent (Fig. 4B). This result indicated that reefs were quickly recolonized, but not by
the same species as those originally present. The compositional differences did not persist, however, and assemblage structure on fish removal reefs became indistinguishable from that on controls after 3 mo (February 1994). The overall community structure on undisturbed or control reefs exhibited little change over
the 2-yr period (relative to the effects of the fish removal disturbance; Fig. 4 A ) , but long-term changes in
total abundance were evident (Fig. 4B).
Both levels of habitat disturbance induced changes
in fish assemblage structure. The strength of these
changes corresponded with the level of disturbance;
the more extreme Level 2 habitat disturbance generated
greater departures from control assemblage composition than did Level 1 disturbance (Fig. 4C). Clearly,
habitat disturbance was responsible for the greatest
change in community structure observed in any of the
treatments. This result was due to a reduction of num-
increase in abundance of small rubble-dwelling carnivores (e.g., Istigobius spp., Parapercis spp., Amblygobiusphalaena), and the damselfishes Chrysipterajlavipinnis and Pomacentrus coelestis (Table 2). There
was no evidence of recovery towards the control species composition over the course of the experiment,
with little temporal change once the new community
structure had developed. Three months after manipulation, overall adult abundances of both habitat disturbance levels were, on average, 15-20 individuals per
reef lower than undisturbed reefs (Fig. 4D). There was
no tendency for a return to the same adult abundances
as control reefs over time, but similar temporal fluctuations in total numbers were observed across all
reefs.
Fish removal in combination with habitat disturbance removed any differences between assemblage
structure and the level of habitat disturbance (Fig. 4E).
However, the overall extent of divergence from control
composition of disturbed reef communities was similar
to that when the original resident fish were present (Fig.
4C). Again, there were no indications of recovery to
the original state, although there was a small, gradual,
and systematic change in community composition over
time. Overall abundance was consistently lower in disturbed reefs relative to their controls (Fig. 4F).
Recruitment
Recruitment differed between reefs with different
levels of habitat disturbance (Habitat, P = 0.0005; Ta-
TABLE2. Structure coefficients of species in the first canonical discriminant (CD 1) axis examining temporal
changes in adult fish abundances.
Species
Pomacentrus moluccensis
Dascvllus reticulatus
~ a s c y l l u sa ruanus
Gobiodon okinalvae
Paragobiodon echinocephalus
Halichoeres melanurus
Amblyglyphidodon curacao
Pomacentrus nagasakiensis
Pseudochromis fuscus
Gobiodon spp.
Pomacentrus amboinensis
Chrysiptera javipinnis
Chrysiptera rollandi
Amblygobius phalaena
Pomacentrus coelestis
Halichoeres trimaculatus
Dischistodus perspicillatus
Parapercis spp.
Correlation
with C D 1
0.487
0.384
0.347
0.335
0.328
0.239
0.202
0.188
0.187
-0.185
-0.198
-0.267
-0.273
-0.337
-0.375
-0.440
Notes: Coefficients are interpretable as simple correlation
coefficients of fish abundance relative to values on the canonical axis. Only species with coefficients greater than 10.181
are included.
CRAIG SYMS AND GEOFFREY P. JONES
Control vs. habitat disturbance
Control vs. fish removal
JASONDJFMAMJJASONDJFMAMJ
1993
1994
Ecology, Vol. 8 1, No. 10
1995
Fish removal alone vs. fish removal
and habitat disturbance
C
E
D
F
JASONDJFMAMJJASONDJFMAMJ
1993
1994
Date
1995
JASONDJFMAMJJASONDJFMAMJ
1993
1994
1995
FIG. 4. Temporal changes in fish community structure contrasting: (A) and (B), fish removal vs, controls; (C) and (D),
habitat disturbance only vs. controls; and (E) and (F), both treatments in combination. Canonical discriminant 1 scores (mean
2 1 SE) reflect species composition changes. For ease of interpretation, we present total adult abundance (mean i 1 SE)
instead of scores on canonical discriminant 2, 0 Control reefs; Fish removal only; O Level 1 habitat disturbance; Level
2 habitat disturbance; r Level 1 habitat disturbance and fish removal; Level 2 habitat disturbance and fish removal. Vertical
line in late October 1993 indicates time of disturbance.
ble 3 ) ; undisturbed controls received greater numbers
of Dascyllus aruanus, Pomacentrus moluccensis, D.
reticulatus, Thalassoma lunare, and Amblyglyphidodon
curacao (Fig. 5). In contrast, reefs on which habitat
was disturbed received greater numbers of Dischistodus perspicillatus. In terms of fish abundance, these
differences were relatively small (Fig. 6). The greatest
absolute change was a shift in numerical dominance
from Pomacentrus nagasakiensis to P. amboinensis
with increasing levels of habitat disturbance (Fig. 6).
Although not statistically significant (Table 3; Removal, P = 0.6345), a shift in composition was indicated
by the C D A (Fig. 5). Reefs from which resident fish
were removed without any disturbance to habitat received fewer Dascyllus aruanus, P. moluccensis, and
D. reticulatus than their corresponding controls.
TABLE3. Multivariate analysis of variance of the total number of recruits received by each reef for the postmanipulative duration of the experiment ( X O . * ~ transformed).
Source
Removal
Habitat
Removal
X
Habitat
Pillai's
trace
df
P
0.3473
1.2440
0.7641
17, 27
34, 56
34, 56
0.6345
0.0005
0.4667
Nore: The Removal treatment entailed a pulse removal of
all fish from the patch reef; the Habitat treatment involved
two levels of habitat destruction.
Species-specific responses
Several distinct species-specific responses were identified. Strongly coral-associated species (e.g., P. moluccensis and D. reticulatus) exhibited dramatic declines
in numbers on habitat disturbed reefs, with no evidence
of recovery in numbers (Fig. 7, Table 4). These species
also did not fully recover from fish removal treatments.
They tended to recruit through larval settlement in very
low numbers although, once established, juveniles persisted throughout the year (Table 4).
Species that were more normally associated with
dead coral surfaces (e.g., P. amboinensis and P. nagasakiensis) recovered rapidly from fish removal
through both settlement and immigration (Fig. 8, Table
4). The abundance of these species peaked shortly after
the disturbances in all treatments. They exhibited moderate declines in abundance on mechanically damaged
reefs relative to controls, but their numbers did not fall
as low as species associated with live coral (cf. Fig.
7). Interestingly, the abundance of P. nagasakiensis on
undamaged reefs increased to greater than control levels following fish removal, indicating the presence of
compensatory settlement/immigration. However, this
trend was temporary and was followed by a substantial
decline which eliminated the effect (Fig. 8D).
Species associated with broken coral and rubble substrata (e.g., Parapercis spp. and Dischistodus perspicillatus) initially increased on damaged reefs, but the
DISTURBANCE EFFECTS ON REEF FISH
October 2000
- 6 - 5 4 - 3 - 2 - 1
0 1 2 3 4
Canonical discriminant 1 (70.14%) 5
6
0.6 D. perspicillatus 0.4 -
f
6
-0.6
gradual decline for the duration of the experiment. A
similar pattern of lower richness was evident on reefs
that received both habitat disturbance and fish removal
(Fig. lOB), although fish removal rendered species
richness of the colonizing community on the two levels
of habitat disturbance indistinguishable. Evenness of
fish species was greater on habitat-disturbed reefs than
on control reefs, regardless of fish removal treatment,
but the level of habitat disturbance did not exert any
effect on evenness (Fig. 10C, D).
Patterns of community response to disturbance have
assumed a central place in ecological theory (Connell
1978, Sousa 1984, Petraitis et al. 1989). However, to
date this theory has not addressed the relative importance of disturbances that remove the focal organisms
(in this case, fishes) vs. disturbance of species that
provide biogenic habitat (in this case, corals). Disturbance appears to be an important process in driving the
dynamics of benthic marine communities, such as coral
reefs (Connell 1978, Huston 1979,1985, Jackson 1991,
Karlson and Hurd 1993). It has not, however, been
prominent in the development of theory addressing the
processes that structure coral-reef fish communities
(see Sale 1991a). Until recently, the perception of reef
fish communities as nonequilibrial assemblages and the
product of stochastic recruitment processes rather than
biological interactions (Doherty 1991, Sale 1991b, Doherty and Fowler 1994) has resulted in a focus on the
unpredictable element of assemblage structure. However, recent evidence suggests that habitat structure can
to a large extent determine the structure of fish assemblages (Hixon and Beets 1993, Ault and Johnson 1998,
Jones and Syms 1998) and biological interactions can
be strong enough to stabilize the constituent populations (Caley et al. 1996, Robertson 1996, Hixon and
Carr 1997). Consequently, the relationship between the
specific effects of disturbance and habitat structure provides a key insight into the organization of reef fish
communities.
Here we proposed that habitat structure was central
to identifying predictable and explainable portions of
variation in reef fish assemblages. Three predictions
followed from this hypothesis: (1) communities subjected to fish mortality alone should return to control
structures; (2) habitat disturbance alone should generate a long-term departure from control assemblage
structure; and (3) a combination of fish mortality with
habitat disturbance should result in the same community structure as habitat disturbance alone. Applying
combinations of fish removal and habitat disturbances
to coral patch-reef fish communities at Lizard Island
tested these predictions.
1
-0.2 -0.4
D. aruanus
2721
P. atnbo'nensis
P:moluccensis
C, schroederi
D. retcculatus
H. rrimacularu
lunare
P. chrysurus
A. curacao
A'. cyanotnos
nagasakiensis
C. rol ndi
6
1
-1.0 -0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0
Correlation with canonical discriminant 1
FIG. 5. Canonical discriminant analysis of recruit abundance pooled across all postmanipulation censuses. (A) Positions of reefs in species-ordinated space. See Fig. 4 for key
to symbols. (B) Structure coefficients (correlations with ordination axes) of species contributing to the ordination pattern. See Table 2 for full species names.
adult numbers did not always persist (Fig. 9, Table 4).
The increase in abundance was initially greatest on
reefs subject to both habitat disturbance and fish removal. Two different categories of response by these
fishes could be identified. Firstly, a number of mobile
carnivorous rubble-dwelling species (Parapercis spp.,
Zstigobius decoratus and Amblygobius phalaena)
moved onto disturbed reefs as adults. A rapid increase
on damaged reefs was followed by a gradual decline
towards the end of the experiment. Secondly, several
damselfishes recruited specifically to disturbed reefs
(Dischistodus perspicillatus, Pomacentrus coelestis,
Chrysiptera JEavipinnis and C. rollandi). These species
settled in relatively high numbers on damaged reefs,
particularly where the residents were also removed, but
juveniles did not persist through the year. Survivorship
(estimated as persistence) appeared lower in the rubbleassociated (Fig. 9) than the coral-associated species
(Fig. 7).
Species richness a n d evenness
The combination of species-specific patterns of loss
and colonization of reefs resulted in a significant overall decline in species richness on reefs subject to habitat
disturbance alone (Fig. 10A). Species richness on control reefs also varied during the experiment, with a
Responses to jish removal a n d habitat disturbance
In contrast to the widely held view that coral-reef
fish communities on patch reefs are disorganized, un-
2722
CRAIG SYMS AND GEOFFREY P. JONES
:q 1
C
A) Control
B) Habitat disturbance Level 1
D) Fish removal only
0
14
-g
12
12
z
10
10
d
9
8
8
$
6
4
6
4
2
2
F1
>
0
.w
G
m
5
14
E) Fish removal and habitat disturbance Level 1
0
O
C) Habitat disturbance Level 2
FIG. 6.
Ecology, Vol. 81, No. 10
Recruit abundance (mean
F) Fish removal and habitat disturbance Level 2
+ 1 SE) pooled across all postmanipulation censuses. See Table 2 for full species names.
predictable systems (Sale 1980, Sale and Steel 1989,
Sale et al. 1994, Ault and Johnson 1998), this study
demonstrated that patch reef assemblages do have a
high degree of coherence. The unmanipulated assemblages on these reefs were persistent through time and,
despite fluctuations in abundance during the study, the
suite of species forming the community remained the
same. Fish removal alone generated only short-term
differences in the assemblages on experimental and
control reefs. Settlement and immigration eventually
removed these differences. This result indicated that
ongoing mechanisms and not temporal autocorrelation
due to fish longevity were responsible for maintaining
the community in a particular state. Two nonmutually
exclusive types of process might be responsible for the
maintenance of these patterns: interactions between the
fishes and their habitat and interactions within the fish
community alone. The community response to fish re-
moval vs. habitat disturbance provided an evaluation
of these alternatives.
Habitat disturbance generated consistent (in the
sense that replicates assumed similar temporal trajectories) and persistent changes in the fish community.
Different levels of habitat disturbance alone resulted
in characteristic community compositions. The extent
of deviation from control assemblages was directly related to the level of habitat destruction. Those assemblages subjected to both fish removal and habitat disturbance also shifted in a similar fashion. However, in
contrast with habitat disturbance alone, there was no
difference between the temporal trajectories of the different levels of disturbance. The relative magnitude of
differences between the habitat disturbance treatments
and control values suggested that fish-habitat interactions were the primary mechanism generating the
pattern, but that resident fish may be able to persist if
October 2000
DISTURBANCE EFFECTS ON REEF FISH
15
Pomacentrus moluccensis
B
A
10
S
FIG. 7. Patterns of change in the abundance
(mean I1 SE) of two abundant species associated with live coral in response to fish removal
and habitat disturbance. See Fig. 4 for key to
symbols. Vertical line in late October 1993 indicates time of disturbance.
2!
>
2 0
;
8
'
Dascyllus reticulatus
C
5
6
4
, ,;,
2
2
:,$,
, , , ,$
-
0-
0
JASONDJFMAMJJASOUDJFMAMJ
1993
1994
JASONDJFMAMJJASONDJFMAMJ
1995
1993
1994
1995
Date
the level of disturbance is below some species-specific
threshold. Changes in the species composition of habitat-disturbed treatments were driven by both declines
in live coral-associated (and some dead coral-associated) species, and increases in rubble-associated species. Habitat disturbance generated a decline in species
richness and an increase in evenness, both of which
were at least partly attributable to the lower abundance
of fish on manipulated reefs.
Demographic mechanisms injuencing community
structure
Demographic responses to fish removal took one of
two forms: immigration of juveniles and adults from
neighboring reefs and larval settlement from the plankton. Although reefs were at least 10 m apart, they were
not effectively isolated. However, immigration did not
completely remove treatment effects. Recolonization
of fish-removal reefs resulted in a total fish abundance
that was indistinguishable from controls, however recolonized reefs had compositional differences which
remained until after the recruitment season. Larval settlement from the plankton provided individuals of species (typically coral associates, Randall et al. 1990)
that appeared to be more reluctant to move between
reefs (e.g., Pomacentrus moluccensis, Dascyllus spp.,
Gobiodon spp.). Habitat choice at settlement appeared
TABLE4. Summary of species-specific responses to different disturbance treatments over the duration of the study.
Species
Pomacentrus moluccensis,
Dascyllus aruanus,
Dascyllus reticulatus
Fish
removal
Habitat
disturbance,
Level 1
Habitat
disturbance,
Level 2
.u-
.u- .u-
uu
Juvenile
settlement
ratio
Juvenile
persistence
low
high (entire study)
U-UU.
high
high (entire study)
low
high (entire study)
l.
low
high (entire study)
Pomacentrus amboinensis,
Pseudochromis fuscus
0
u.
u
u.
Pomacentrus nagasakiensis
0
0
Chrysiptera rollandi,
Parapercis spp.,
Halichoeres trimaculatus
0
n
I?
moderate
moderate
high (entire study)
low (4 mo)
Chrysiptera javipinnis,
Pomacentrus coelestis
0
I?
fill
high
low (4mo)
Dischistodus perspicillatus
0
nil
fill
high
moderate (9 mo on
disturbed reefs)
Amblyglyphidodon curacao
0
Halichoeres melanurus
.u-
u,
.u-
Notes: Definition of arrow symbols: reduction in abundance; U-d, strong reduction in abundance; fi, increase in abundance;
in abundance; 0 , no change. Juvenile settlement ratio is the ratio of recruit to adult abundance at any
one census.
flfi, strong increase
CRAIG SYMS AND GEOFFREY P. JONES
Ecology, Vol. 81, No. 10
Pomacentrias amboinensis
B
20
16
12
8
4
-S
FIG. 8. Patterns of change in the abundance
(mean t 1 SE) of two abundant species associated with dead coral substrata in response to
fish removal and habitat disturbance. See Fig.
4 for key to symbols. The vertical line in late
October 1993 indicates time of disturbance.
0
Pomacentrus nagasakiensis
JASOND JFMAMJ JASONDJFMAMJ
1993
1994
JASOND JFMAMJ JASONDJFb1,AMJ 1995
1993
1994
1995
Date
to have been largely responsible for these patterns, and
such habitat selection would have been operating at
reasonably small scales (a few square meters). A weak
(statistically nonsignificant) positive effect of resident
fauna on recruit numbers was indicated for coral-associates on reefs that did not receive any habitat disturbance (previously noted by Sweatman 1985 for Dascyllus aruanus), but had no effect on the resulting adult
abundance of these species. The absence of strong positive or negative priority effects indicated that strong
interactions between the resident fauna and subsequent
colonists (e.g., predation, competition) were not as important as habitat in determining the community structure (cf. Shulman et al. 1983).
3.0
2.5
2.0
1.5
1.0
0.5
0.0
Parapercis spp.
B
3.0
2.5
2.0
1.S
1.0
0.5
0.0
A
.
'CI
$
$
The species that typified the assemblages on undisturbed and habitat-disturbed reefs appeared to have different demographic rates. Coral associates (e.g., P.
moluccensis and Dascyllus reticulatus) typically recruited from the plankton in low numbers, but survivorship was relatively high. In contrast, species more
normally associated with dead coral surfaces (e.g., Pomacentrus amboinensis and P. nagasakiensis) settled
in greater numbers, but with considerable post-settlement mortality which, especially in P. amboinensis,
increased with extreme levels of habitat disturbance.
Species associated with broken coral and rubble substrata exhibited two types of demographic response.
Immigration was the primary colonization mechanism
b)
FIG. 9. Patterns of change in the abundance
(mean i: 1 SE) of two abundant species associated with rubble in response to fish removal
and habitat disturbance. See Fig. 4 for key to
symbols. The vertical line in late October 1993
indicates time of disturbance.
Dischistodus perspicillatus
D
JASONDJFMAMJ JASONDJFMAMJ 1993
1994
1995
1993
Date
1994
1995
October 2000
DISTURBANCE EFFECTS ON REEF FISH
FIG. 10. Patterns of change (mean f 1 SE)
in (A and C), species richness and (B and D),
evenness, in response to fish removal and habitat disturbance. See Fig. 4 for key to symbols.
The vertical line in late October 1993 indicates
time of disturbance.
o!,
,
, ! ,, , , , , , , , , , , , , , ,,,
J A S O N D J F M A M J JASONDJFMAM J
1993
1994
o.o,.,,,,,,,,,,,,,.,,,,.,,,
JASONDJFMAMJ JASONDJFMAMJ
1995
1993
1994
1995
Date
for Parapercis spp., Zstigobius decoratus and Amblygobius phalaena which moved onto disturbed reefs as
adults whereas several damselfishes characteristic of
disturbed reefs (Dischistodus perspicillatus, Pomacentrus coelestis, Chrysiptera flavipinnis, and C. rollandi)
settled in high numbers but had typically low survivorship.
The covariation between the disturbance agent and
demographic responses has two important consequences for modeling coral-reef fish community dynamics.
First, recolonization of species that move into disturbed
habitats as adults may occur over more restricted scales
than those of species which settle from the plankton
(Syms and Jones 1999). In addition, the spatial extent
of habitat disturbance may interact with specific habitat
cues at settlement (Syms and Jones 1999). Second,
mathematical modeling of the system will need to incorporate some measure of covariation between habitat
and local dynamics (i.e., "birth" and death rates) of
different sorts of patches. Variable environment theory
(Chesson 1994) provides a framework within which
this can be incorporated, but development of a realistic
model will require considerable empirical parameterization of the relationship between patch type and local
population dynamics on patches of a given type.
A revised view of the processes structuring
coral-reef fish communities
The results from this study support a model of patchreef fish assemblages as a product primarily of habitatmediated processes, which appear to constrain the community and most of the constituent populations. Fish
mortality and habitat disturbance asserted additive effects (as indicated by a lack of significant interaction)
to yield a consistent average patch response contingent
on the level of disturbance. The underlying mechanisms explaining this pattern may include species-specific differences in habitat selection both at settlement
(Sale et al. 1984, Ohman et al. 1998) and through subsequent migration (Booth and Beretta 1994, Lewis
1997b). Interspecific interactions that are mediated by
habitat structure (especially predation) or resource requirements would also contribute to responses to habitat disturbance (Shulman 1985, Jones 1988b, Hixon
and Beets 1993, Forrester 1995, Hixon and Carr 1997,
Beukers and Jones 1998).
Our conclusion, on face value, appears counter to
previous studies which have characterized reef fish assemblages as highly unpredictable assemblages (Sale
1977, 1980), or recruit-limited to the extent that density-dependent interactions are relatively unimportant
(Doherty and Williams 1988). On closer examination,
this is not necessarily the case as both deterministic
and stochastic factors are likely to contribute to the
observed pattern. The lack of strong association between patch-reef fish assemblages and habitat variables
has been cited as evidence that habitat is not important
in structuring fish assemblages (e.g., Sale and Douglas
1984, Sale et al. 1994, Ault and Johnson 1998). Measurement of habitat association is contingent on scale
(Syms 1995), and while all fish ecologists acknowledge
larger scale physiographic or zonal differences in fish
assemblages (e.g., Williams 1991), the role of finer
scale (operating at spatial scales of a few meters) habitat characters has been more widely debated (Gladfelter and Gladfelter 1978, Ogden and Ebersole 1981,
Roberts and Ormond 1987). The strength of organismhabitat association is also contingent on the range of
the habitat variables over which the association is measured (Jones and Syms 1998). In an experiment in
which replicates are chosen so as to be similar to each
other, it is probably unreasonable to expect strong patterns within the (premanipulated) sample units because
habitat variability has been actively reduced. Indeed in
this study, no preexisting habitat association was apparent, and habitat "determinism" only became apparent after an experimentally induced habitat gradient
was generated.
Early formulations of nonequilibrial models of coral-
2726
CRAIG SYMS AND GEOFFREY P. JONES
reef fish communities (Sale 1977, Victor 1983) took as
their initial observation the fact that a large portion of
the variability of fish communities was unexplainable.
Notwithstanding the analytical problems of measuring
community concordance through time (Rahel et al.
1984, Ebeling et al. 1990, Rahel 1990), it appears in
the majority of studies that predictions of species composition and fish abundance over time are imprecise.
We do not disagree with this view. The analytical method used in this study isolated that portion of variation
explainable by the experimental factors. The greatest
portion (46.6%) of variability in adult numbers was
attributable to differences between treatments over
time, 37.4% of which was due to differences in species
composition and the remaining 9.2% attributable to
fluctuations in temporal abundance. Within-reef variability (i.e., the blocking factor) was highly significant
and, in combination with residual variation, explained
the remaining 53.4% of variation. In other words, more
than half the variation was attributable to unexplained,
possibly stochastic factors.
This study was carried out on relatively small habitat
patches which were "open" with respect to larval supply (i.e., larval availability was not a function of resident fish fecundity). Although patch reefs are a significant component of coral reef systems, particularly
in back reef areas, the effect of scale on their utility
as a model of the coral reef system as a whole has been
debated (Ogden and Ebersole 1981, Sale and Douglas
1984). Scale is a problem inherent in studies conducted
on habitat patches, and unfortunately, in coral reef systems (and marine reef systems in general) little work
has been done to identify the potential effects of scale
on experimental interpretation (but see Syms and Jones
1999). However, most of the species that exist on patch
reefs do so for the duration of their adult lives. Consequently, the scale at which they exert habitat preferences and interact with both conspecifics and interspecific individuals (i.e., their ecological neighborhood, Addicott et al. 1987) is that of the patch reef.
The potential interaction between the deterministic
and stochastic portions of variation apparent at different scales has wide theoretical implications. The central
role of habitat as a mediator of interactions between
individuals provides a likely mechanism by which density-dependence can operate on a local scale to regulate
large-scale dynamics (Chesson 1997, 1998). In particular, reef crevices may serve as prey refuges and reef
microhabitat may modify the strength and direction of
competitive interactions. In addition, the large-scale
strength of these processes could be modeled by integrating across the range of different habitat types over
which populations and communities are fragmented to
yield a mosaic-level model. Spatial (Chesson 1985) and
temporal (Chesson 1981, Chesson and Warner 1981)
variability are likely to interact with density-dependent
processes to promote coexistence by a spatiotemporal
Ecology, Vol. 81, No. 10
"storage effect" (Chesson 1985, Warner and Chesson
1985).
Conclusions
This study suggests an alternative view of coral-reef
fish assemblages as systems structured by both deterministic and stochastic processes. This view appears
to counter the recent stochastic paradigm, but on closer
examination may be seen as a shift in focus from the
unpredictable to the predictable portion of variability.
Habitat mediated a significant portion of community
structure, indicating that the constituent populations
were constrained within broad limits by their habitat
requirements and the potential covariance of habitat
with intra- and interspecific interactions. When habitats
change in structure as a result of different regimes of
disturbance, so will the fish community. When fish
communities suffer direct mortality, areas with similar
habitat availability will become more similar in their
new fish assemblages over time. Certainly, stochastic
variation in recruitment and migration may be responsible for the considerable variability in community
structure that occurs within the limits set by the habitat.
However, while unexplainable variation is important in
an inherently variable system, it is the explainable portion of variance that provides the soundest platform
from which to develop a predictive theory of ecology.
We thank the numerous people who assisted us in the field
and the staff of the Lizard Island Research Station for their
support. Thanks also to Tara Anderson who assisted in the
preparation of the figures. Various stages of this manuscript
benefited from the comments of Tara Anderson, Mark Carr,
Peter Chesson, Mark Hixon, Mick Keough, Peter Sale, and
two anonymous reviewers. This research was supported by
an Australian Research Council Large Grant to G. P. Jones.
LITERATURE
CITED
Addicott, J. E , J. M. Aho, M. E Antolin, D. K. Padilla, J. S.
Richardson, and D. A. Soluk. 1987. Ecological neighborhoods: scaling environmental patterns. Oikos 49:340-346.
Ault, T. R., and C. R. Johnson. 1998. Spatially and temporally
predictable fish communities on coral reefs. Ecological
Monographs 68:25-50.
Bell, J. D., and R. Galzin. 1984. Influence of live coral cover
on coral-reef fish communities. Marine Ecology Progress
Series 15:265-274.
Bell, J., M. Harmelin-Vivien, and R. Galzin. 1985. Large
scale spatial variation in abundance of Butterflyfishes
(Chaetodontidae) on Polynesian reefs. Proceedings of the
Fifth International Coral Reef Congress 5:421-426.
Beukers, J. S . , and G. P. Jones. 1998. Habitat complexity
modifies the impact of piscivores on a coral reef fish population. Oecologia 114:50-59.
Bodkin, J. L. 1988. Effects of kelp forest removal on associated fish assemblages in central California. Journal of
Experimental Marine Biology and Ecology 117:227-238.
Bohnsack, J. A. 1983. Resiliency of reef fish communities
in the Florida Keys following a January 1977 hypothermal
fish kill. Environmental Biology of Fishes 9:41-53.
Booth, D. J., and G. A. Beretta. 1994. Seasonal recruitment,
habitat associations and survival of pomacentrid reef fish
in the US Virgin Islands. Coral Reefs 13:81-89.
Bouchon-Navaro, Y., and C. Bouchon. 1989. Correlations
October 2000 DISTURBANCE EFFECTS ON REEF FISH
between chaetodontid fishes and coral communities o f the
Gulf o f Aqaba (Red Sea). Environmental Biology o f Fishes
25:47-60.
Bouchon-Navaro, Y., C . Bouchon, and M . L. Harmelin-Vivien. 1985. Impact o f coral degradation on a chaetodontid
fish assemblage (Moorea, French Polynesia). Proceedings
o f the Fifth International Coral Reef Congress, Tahiti 5 :
427-432.
Caley, M . J., M. H. Carr, M. A . Hixon, T. P. Hughes, G . P.
Jones, and B. A . Menge. 1996. Recruitment and the local
dynamics o f open marine populations. Annual Review o f
Ecology and Systematics 27:477-500.
Carr, M. H. 1989. Effects o f macroalgal assemblages on the
recruitment o f temperate zone reef fishes. Journal o f Experimental Marine Biology and Ecology 126:59-76.
Carr, M. H. 1991. Habitat selection and recruitment o f an
assemblage o f temperate zone reef fishes. Journal o f Experimental Marine Biology and Ecology 146: 113-137.
Chesson, P. L. 1981. Models for spatially distributed population: the e f f e c t o f within-patch variability. Theoretical
Population Biology 19:288-325.
Chesson, P. L. 1985. Coexistence o f competitors in spatially
and temporally varying environments: a look at the combined effects o f different sorts o f variability. Theoretical
Population Biology 28:263-287.
Chesson, P. L. 1994. Multispecies competition in variable
environments. Theoretical Population Biology 45:227-276.
Chesson, P. L. 1997. Diversity maintenance by integration
o f mechanisms over various scales. Proceedings o f the
Eighth International Coral Reef Symposium 1:405-410.
Chesson, P. L. 1998. Spatial scales in the study o f reef fishes:
a theoretical perspective. Australian Journal o f Ecology 23:
209-215.
Chesson, P. L., and N. Huntly. 1997. The roles o f harsh and
fluctuating conditions in the dynamics o f ecological communities. American Naturalist 150:519-553.
Chesson, P. L., and R. R. Warner. 198 1. Environmental variability promotes coexistence in lottery competitive systems. American Naturalist 125:923-943.
Choat, J. H., and A . M. Ayling. 1987. The relationship between habitat structure and fish faunas on New Zealand
reefs.Journal o f Experimental Marine Biology and Ecology
110:257-284.
Clark, J . S. 1991. Disturbance and population structure on
the shifting mosaic landscape. Ecology 7 2 :11 19-1 137.
Connell, J . H. 1978. Diversity in tropical rain forests and
coral reefs. Science 199:1302-13 10.
Cox, E. E 1994. Resource use by corallivorous butterflyfishes
(Family Chaetodontidae) in Hawaii. Bulletin o f Marine Science 54:535-545.
Dayton, P. K., and R . R. Hessler. 1972. Role o f biological
disturbance in maintaining diversity in the deep sea. Deep
Sea Research 19:199-208.
DeMartini, E. E., and D. A . Roberts. 1990. Effects o f giant
kelp (Macrocystis) on the density and abundance o f fishes
in a cobble-bottom kelp forest. Bulletin o f Marine Science
46:287-300.
Doherty, P. J . 1983. Tropical territorial damselfishes: is density limited by aggression or recruitment? Ecology 64:176190.
Doherty, P. J. 1991. Spatial and temporal patterns in recruitment. Pages 261-293 in P. F. Sale, editor. The ecology o f
fishes on coral reefs. Academic Press, San Diego, California, U S A .
Doherty, P. J., and A . Fowler. 1994. A n empirical test o f
recruitment limitation in a coral reef fish. Science 263:935939.
Doherty, P. J., and D. McB. Williams. 1988. The replenishment o f coral reef fish populations. Oceanography and Marine Biology: An Annual Review 26:487-55 1.
2727
Dollar, S. J . , and G . W . Tribble. 1993. Recurrent storm disturbance and recovery: a long-term study o f coral communities in Hawaii. Coral Reefs 12:223-233.
Dutilleul, P. 1993. Spatial heterogeneity and the design o f
ecological field experiments. Ecology 74:1646-1658.
Ebeling, A . W . , S. J. Holbrook, and R . J . Schmitt. 1990.
Temporally concordant structure o f a fish assemblage:
bound or determined? American Naturalist 135:63-73.
Findley, J. S., and M. T. Findley. 1985. A search for pattern
in butterfly fish communities. American Naturalist 126:
800-816.
Forrester, G . E. 1995. Strong density-dependent survival and
recruitment regulate the abundance o f a coral reef fish.
Oecologia 103:275-282.
Fowler, A . J. 1990. Spatial and temporal patterns o f distribution and abundance o f chaetodontid fishes at One Tree
Reef, southern G B R . Marine Ecology Progress Series 64:
39-53.
Gladfelter,W . B., and E. H. Gladfelter. 1978. Fish community
structure as a function o f habitat structure on West Indian
patch reefs. Revista de Biologica Tropical 26:65-84.
Green, A . L. 1996. Spatial, temporal and ontogenetic patterns
o f habitat use by coral reef fishes (Family: Labridae). Marine Ecology Progress Series 133:1-1 1.
Harmelin-Vivien, M. L., and P. Laboute. 1986. Catastrophic
impact o f hurricanes on atoll outer reef slopes in the Tuamotu (French Polynesia). Coral Reefs 5:55-62.
Hart, A . M., D. W . Klumpp, and G . R . Russ. 1996. Response
o f herbivorous fishes to crown-of-thorns starfish Acanthaster planci outbreaks. 11. Density and biomass o f selected species o f herbivorous fish and fish-habitat correlations. Marine Ecology Progress Series 132:21-30.
Hassell, M. P., T. R. E. Southwood, and P. M . Reader. 1987.
The dynamics o f the viburnum whitefly (Aleurotrachelus
jelinekii): a case study o f population regulation. Journal o f
Animal Ecology 56:283-300.
Hixon, M. A . 1991. Predation as a process structuring coral
reef fish communities. Pages 475-508 in P. E Sale, editor.
The ecology o f fishes on coral reefs. Academic Press, San
Diego, California, U S A .
Hixon, M . A. 1998. Population dynamics o f coral-reef fishes:
controversial concepts and hypotheses. Australian Journal
o f Ecology 23:192-201.
Hixon, M . A , , and J . P. Beets. 1993. Predation, prey refuges,
and the structure o f coral-reef fish assemblages. Ecological
Monographs 63:77-101.
Hixon, M . A., and M. H. Carr. 1997. Synergistic predation,
density dependence, and population regulation in marine
fish. Science 277:946-949.
Holbrook, S. J., R. J. Schmitt, and R . E Ambrose. 1990.
Biogenic habitat structure and characteristics o f temperate
reef fish assemblages. Australian Journal o f Ecology 15:
489-503.
Hughes, T. P. 1994. Catastrophes, phase shifts, and largescale degradation o f a Caribbean coral reef. Science 265:
1547-1551.
Huston, M. 1979. A general hypothesis o f species diversity.
American Naturalist 113:81-101.
Huston, M . A . 1985. Patterns o f species diversity on coral
reefs. Annual Review o f Ecology and Systematics 16:149177.
Jackson, J . B . C. 1991. Adaptation and diversity o f reef corals. Bioscience 41:475-482.
Jones, G . P. 1988a. Ecology o f rocky reef fish o f north-eastern
New Zealand: a review. New Zealand Journal o f Marine
and Freshwater Research 22:445-462.
Jones, G . P. 1988b. Experimental evaluation o f the effects o f
habitat structure and competitive interactions on the juveniles o f two coral reef fishes. Journal o f Experimental
Marine Biology and Ecology 123: 115-126.
October 2000
DISTURBANCE EFFECTS ON REEF FISH
fish communities on the reef slope. Journal of Experimental
Marine Biology and Ecology 230: 15 1-167.
Syms, C. and G. P. Jones. 1999. Scale of disturbance and the
structure of a temperate fish guild. Ecology 80:921-940.
Victor, B. C. 1983. Recruitment and population dynamics of
a coral reef fish. Science 219:419-420.
Victor, B. C. 1986. Larval settlement and juvenile mortality
in a recruitment-limited coral reef fish population. Ecological Monographs 56: 145-160.
2729
Walsh, W. J. 1983. Stability of a coral reef fish community
following a catastrophic storm. Coral Reefs 2:49-63.
Warner, R. R., and P. L. Chesson. 1985. Coexistence mediated
by recruitment fluctuations: a field guide to the storage
effect. American Naturalist 125:769-787.
Williams, D. McB. 199 1. Patterns and processes in the distribution of coral reef fishes Pages 437-474 in P. F. Sale,
editor. The ecology of fishes on coral reefs. Academic
Press, San Diego, California, USA.