Ecology, 92(12), 2011, pp. 2285–2298� 2011 by the Ecological Society of America

Habitat biodiversity as a determinant of fish community structureon coral reefs

VANESSA MESSMER,1,2,3,6 GEOFFREY P. JONES,1,2 PHILIP L. MUNDAY,1,2 SALLY J. HOLBROOK,4,5 RUSSELL J. SCHMITT,4,5

AND ANDREW J. BROOKS4

1School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811 Australia2ARC Centre of Excellence for Coral Reef Studies, James Cook University, Queensland 4811 Australia

3USR 23278 CNRS-EPHE, Centre de Recherches Insulaires et Observatoire de l’Environnement (CRIOBE),Universite de Perpignan, BP 1013, 98729 Moorea, French Polynesia

4Marine Science Institute, University of California, Santa Barbara, California 93106 USA5Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California 93106 USA

Abstract. Increased habitat diversity is often predicted to promote the diversity of animalcommunities because a greater variety of habitats increases the opportunities for species tospecialize on different resources and coexist. Although positive correlations between thediversities of habitat and associated animals are often observed, the underlying mechanismsare only now starting to emerge, and none have been tested specifically in the marineenvironment. Scleractinian corals constitute the primary habitat-forming organisms on coralreefs and, as such, play an important role in structuring associated reef fish communities.Using the same field experimental design in two geographic localities differing in regional fishspecies composition, we tested the effects of coral species richness and composition on thediversity, abundance, and structure of the local fish community. Richness of coral speciesoverall had a positive effect on fish species richness but had no effect on total fish abundanceor evenness. At both localities, certain individual coral species supported similar levels of fishdiversity and abundance as the high coral richness treatments, suggesting that particular coralspecies are disproportionately important in promoting high local fish diversity. Furthermore,in both localities, different microhabitats (coral species) supported very different fishcommunities, indicating that most reef fish species distinguish habitat at the level of coralspecies. Fish communities colonizing treatments of higher coral species richness represented acombination of those inhabiting the constituent coral species. These findings suggest thatmechanisms underlying habitat–animal interaction in the terrestrial environment also apply tomarine systems and highlight the importance of coral diversity to local fish diversity. The lossof particular key coral species is likely to have a disproportionate impact on the biodiversity ofassociated fish communities.

Key words: biodiversity; climate change; coral reefs; diversity patterns; Great Barrier Reef, Australia;habitat–animal interactions; habitat loss; Kimbe Bay, northern Papua New Guinea; reef fish; resources;species richness.

INTRODUCTION

A fundamental issue in ecology is to understand the

key processes that establish and maintain patterns in

biodiversity. Although many hypotheses have been put

forward to explain differences in biodiversity at large

spatial scales, such as climatic factors, environmental

stability, land area, habitat heterogeneity, historical

influences, and energy availability (Kerr and Packer

1997), the underlying mechanisms remain largely

untested. Yet, biodiversity is increasingly argued to be

crucial in providing and maintaining ecosystem services

(Loreau et al. 2001, Hooper et al. 2005, Mora et al.

2011). Hence, understanding the causes and consequenc-

es of biodiversity loss requires urgent attention. Habitat

loss is widely recognized as a main driver of declining

biodiversity, particularly for terrestrial environments

(Vitousek et al. 1997, Fahrig 2001, Laurance 2007). In

many instances, habitat is transformed to a state of

lower diversity and complexity, rather than being lost

completely. Consequently, determining to what extent

the local diversity of animal communities is dependent

on habitat diversity is critical for predicting the outcome

of ongoing habitat modification and degradation (Tews

et al. 2004).

Positive correlations between the diversities of habitat

and associated animal communities have often been

observed (Lawton 1983, Tews et al. 2004, Kissling et al.

2008, Hortal et al. 2009), although occasionally no

(Currie 1991) or negative relationships (Ralph 1985)

have also been reported. In the terrestrial environment,

Manuscript received 7 January 2011; revised 10 May 2011;accepted 10 June 2011. Corresponding Editor: J. R. Rooker.

6 Present address: ARC Centre of Excellence for CoralReef Studies, James Cook University, Queensland 4811Australia. E-mail: vanessa.messmer@gmail.com

2285

these relationships are usually based on plants, which

act as the primary habitat-forming organisms, and their

associated animals, often herbivores (Lawton 1983,

Currie 1991, Tews et al. 2004, Wolters et al. 2006, Jetz

et al. 2009), but cascading effects across trophic levels

can also occur (Knops et al. 1999, Crutsinger et al.

2006). For example, increased genotypic diversity in

plants was found to have positive effects on the diversity

of herbivorous insects, which in turn was correlated with

predator diversity (Crutsinger et al. 2006).

Attempts to explain the underlying mechanisms for

positive habitat–animal diversity relationships have

produced three main hypotheses (Kissling et al. 2008,

Jetz et al. 2009). (1) The ‘‘producer–consumer hypoth-

esis’’ assumes that animal species compete for food and

usually display some degree of resource specialization.

Higher diversity in food species therefore would

promote niche diversification and coexistence of diverse

consumers (Hutchinson 1959, Chesson 2000, Novotny et

al. 2006). (2) The ‘‘vegetation (habitat) structure

hypothesis’’ predicts that plant diversity may increase

structural or habitat complexity, thereby providing more

physical niches for animals to coexist (Tews et al. 2004).

(3) The habitat–animal diversity relationship may have

no direct causality and instead may arise from both

groups responding similarly to external factors, such as

environmental conditions (Hawkins and Porter 2003).

These mechanisms are not mutually exclusive and may

indeed act synergistically. However, a direct causal effect

vs. similar responses to environmental variables has very

different implications for conservation planning and is

fundamental to understanding how ecosystems work.

To date, few studies have attempted to experimentally

resolve the mechanisms underlying positive relationships

between habitat and animal diversity, and almost all of

this work has been conducted in terrestrial systems.

Tropical coral reefs present an ideal system to test the

proposed explanations because they are one of the most

diverse ecosystems in existence and large-scale correla-

tions between species richness of corals (the primary

habitat-forming organisms) and species richness of fishes

have been well documented along latitudinal and

longitudinal gradients (Briggs 1999, Hughes et al.

2002, Bellwood and Meyer 2009). The global degrada-

tion of coral reefs and detrimental effects on the

diversity and abundance of fish communities as a

consequence of loss in coral cover and structural

complexity (McClanahan 2002, Jones et al. 2004,

Graham et al. 2006, Wilson et al. 2006, Pratchett et al.

2008) highlight the importance of live corals for

associated animal communities. A better understanding

is necessary if we are to design effective conservation

strategies. Although it is highly unlikely that a single

process determines patterns of biodiversity on coral

reefs, the relative contribution of habitat variables in

shaping correlation among species patterns compared to

external variables, such as energy, climate, and historical

factors, has received very little attention. One exception

assessed how the mid-domain effect (overlap between

species ranges), energy supply (sea surface temperatures

and primary productivity), environmental variability

(changes in sea surface temperatures), and habitat

availability (habitat area, coastline length, and number

of coastal islands) predicted latitudinal diversity gradi-

ents in shore fishes using spatial autocorrelations (Mora

and Robertson 2005). In contrast to a number of

terrestrial studies (Kerr and Packer 1997, Hawkins and

Porter 2003, Jetz et al. 2009), environmental variability

and energy supply were not found to influence fish

diversity gradients. The mid-domain effect seemed to be

the strongest determinant for widespread species, and

habitat availability played an important role in small-

range species (Mora and Robertson 2005). However, the

effects of habitat diversity were not addressed and its

functional role in maintaining the diversity of associated

animals in the marine environment is unknown and has

never been experimentally tested.

We expect coral biodiversity to play an important role

in promoting diverse fish assemblages. Live coral cover

and topographic complexity of reef habitat, in particu-

lar, are critical for associated fishes and appear to have a

significant positive influence on reef fish diversity

(Luckhurst and Luckhurst 1978, Bell and Galzin 1984,

Roberts and Ormond 1987, Ohman and Rajasuriya

1998, Holbrook et al. 2008), but the effects of coral

diversity are less well known. Niche differentiation is

likely to be common among reef fishes, as varying

degrees of specialization on corals as a resource for food

or shelter exist between reef fish species (Munday 2004,

Cole et al. 2008, Pratchett and Berumen 2008).

Approximately 9–11% are strictly dependent on live

coral (Jones et al. 2004, Pratchett et al. 2008), and two-

thirds of coral reef fish are only found at sites with some

live coral (Bell and Galzin 1984). The strongest

associations with a particular coral species are generally

found for coral reef fish with specialized resource

requirements, such as obligate coral-dwelling (e.g.,

species of Gobiodon) (Munday et al. 1997) or coral-

feeding fishes (e.g., many species of Chaetodon) (Pratch-

ett and Berumen 2008). Other fish species may simply

prefer certain coral species as important shelter or

recruitment sites (Holbrook et al. 2002, Jones et al.

2004). Some fishes only associate with particular coral

species (Sale 1991, Munday 2004, Gardiner and Jones

2005) and different coral species have been shown to

support different fish communities (Holbrook et al.

2002, Feary et al. 2007). High levels of dependency on

the coral habitat suggest that niche differentiation (in

both food and shelter) is common among reef fishes, and

we would therefore predict a direct causal effect of coral

diversity on fish diversity.

In this study, field experiments were used to assess for

the first time the potential causal relationship between

the local biodiversity of corals and their associated fish

assemblages by isolating this effect from any environ-

mental variables. Specifically, the following two hypoth-

VANESSA MESSMER ET AL.2286 Ecology, Vol. 92, No. 12

eses were tested. (1) There is a direct causal link between

habitat diversity and the diversity of associated animals

on coral reefs, i.e., coral species richness is a primary

determinant of local reef fish species richness, diversity,

and abundance. (2) Niche partitioning is an importantprocess underlying the relationship between habitat

diversity and associated animal diversity, i.e., different

coral species support different fish assemblages, with the

consequence that fish community composition is depen-

dent on the presence of particular coral species. If the‘‘producer–consumer hypothesis’’ prevails, we would

only expect species directly feeding on coral to respond

to habitat diversity. In the ‘‘habitat structure hypothe-

sis,’’ habitat selection for shelter and living space would

play a major role, whereas a similar response to

environmental factors (hypothesis three) may be as-sumed if no causal link is found. To determine whether

local patterns were robust to regional differences in fish

species composition or fish–habitat interactions, the

experiment was repeated in two locations; Kimbe Bay in

Papua New Guinea, and Lizard Island on the GreatBarrier Reef, Australia. Similarly high levels of coral

and fish diversity, but substantial differences in fish

community structure, characterize the two locations.

METHODS

Experimental design and protocols

To test the effects of coral diversity on fish commu-

nities, experiments were conducted in the lagoons ofLizard Island on the Great Barrier Reef, Australia

(148410 S, 1458270 E) and Schumann Island in Kimbe

Bay, northern Papua New Guinea (58310 S, 150850 E)

(Appendix : Fig. A1). In each location, 45 patch reefs

were constructed using a total of six common, coexistingcoral species that had a branching morphology (Table

1). To examine the effects of coral species richness on

fish community characteristics, individual patch reefs

were composed of one, three, or six coral species. To

examine the effects of coral species composition on fish

assemblages, the single-species treatment was repeated

for each of the six coral species, and two medium-

diversity treatments were established using two different

combinations of three coral species, with each coral

species assigned to only one of the medium treatments

(see Table 1 for species combinations). All nine

treatments were replicated five times. The volume of

live coral was kept as constant as possible across

treatments. Four species were the same at both locations

(Acropora nasuta, Pocillopora damicornis, Porites cylin-

drica, and Seriatopora hystrix). Two similar species were

used to represent staghorn Acropora (A. muricata at

Lizard Island; A. grandis at Kimbe Bay) and bottlebrush

Acropora (A. loripes at Lizard Island; A. carduus in

Kimbe Bay); see Table 1. For simplicity, we refer to the

different treatments with codes: Acropora nasuta (An),

bottlebrush Acropora (Bb), Porites cylindrica (Pc),

Pocillopora damicornis (Pd), Seriatopora hystrix (Sh),

staghorn Acropora (St), medium combination A (MA),

medium combination B (MB), and high (H).

Patch reefs, each 100 cm in diameter and 50 cm high,

were built at 3–7 m depth on large, flat, sandy areas

where no other habitat structure was present. Reefs were

placed 15 m apart from each other and from any

neighboring reef structures to limit fish movement

between reefs. The base of each patch reef consisted of

dead coral rubble, which was covered with the same

amount of live coral for each patch reef (90% live coral

cover). Patch reefs were established in April 2007 in

Kimbe Bay and in November 2007 at Lizard Island.

Fish were allowed to naturally colonize the patch reefs

over a 12-month period and the patch reefs were

surveyed four times, i.e., every 3–5 months. For each

survey, the abundance of every fish species present on

each reef was recorded. Recorded fish species included

all those associated with the patch reefs, but did not

include larger mobile species that were observed to move

on a regular basis between reefs. Minor repairs to the

reefs were carried out where necessary after each survey.

Commencement of the experiment at each location was

timed to match the start of the respective recruitment

TABLE 1. List of the coral species and number of coral species used in each treatment at Lizard Island, Great Barrier Reef,Australia, and at Kimbe Bay, Papua, New Guinea.

Treatment CodeDiversity(no. spp.) Lizard Island Kimbe Bay

Single species

A. nasuta An 1 Acropora nasuta Acropora nasuta‘‘Staghorn’’ St 1 Acropora muricata Acropora grandis‘‘Bottlebrush’’ Bb 1 Acropora loripes Acropora carduusP. damicornis Pd 1 Pocillopora damicornis Pocillopora damicornisP. cylindrica Pc 1 Porites cylindrica Porites cylindricaS. hystrix Sh 1 Seriatopora hystrix Seriatopora hystrix

Medium A MA 3 A. loripes, P. damicornis, P. cylindrica A. carduus, P. damicornis, P. cylindricaMedium B MB 3 A. nasuta, A. muricata, S. hystrix A. nasuta, A. grandis, S. hystrixHigh H 6 A. nasuta, A. muricata, A. loripes, P.

damicornis, P. cylindrica, S. hystrixA. nasuta, A. grandis, A. carduus, P.

damicornis, P. cylindrica, S. hystrix

Notes: Patch reefs were characterized by three different levels of coral species richness (1, 3, and 6 species). The single-speciestreatments were repeated for all six coral species, and two combinations of three coral species were used for the medium-diversitytreatments. The high-diversity treatment included all six coral species used at each location.

December 2011 2287CORAL REEF HABITAT AND FISH DIVERSITY

seasons. Recruitment is highest during the dry winter

season in Kimbe Bay, whereas a distinct recruitment

peak occurs over summer at Lizard Island. Fish species

richness and abundance patterns were mostly estab-

lished after 2 months at both locations (V. Messmer,

unpublished data). Because the patch reefs in Kimbe Bay

were in a deteriorated state during the last survey, results

presented here are from the survey carried out in late

November 2007 (8 months), coinciding with the end of

the recruitment season. The 12-month survey at Lizard

Island (early December 2008) coincided with the peak of

the recruitment season and was therefore the most

comparable survey.

Statistical analyses

Fish communities at Lizard Island and Kimbe Bay

were very different, with only 24.2% of recorded species

shared between locations (Appendix : Fig. A2). Analy-

ses were therefore carried out separately for each

location. Mean fish species richness and abundance

were based on the total number of species or individuals

observed on each replicate reef during the last survey

and were averaged (1) for each level of coral species

richness or (2) for each treatment. First, the effects of

coral species richness on fish species richness, evenness,

and abundance were compared between three richness

levels of coral species (low, medium, high). For this

analysis, fish species richness and abundance were

pooled and averaged across the six single-coral species

treatments (low) and for both three-coral-species treat-

ments (medium) and for the six-coral-species plots

(high). Second, to test the effects of coral identity on

fish assemblages, fish species richness, evenness, and

abundance were analyzed separately for each treatment

(nine levels). One-way ANOVA, followed by Tukey’s

hsd post hoc tests, compared differences in fish species

richness, arcsine-transformed fish species evenness

(Shannon evenness index, J ), and total fish abundance.

To determine the influence of different coral species

and coral species richness on the composition of fish

communities (i.e., species composition and relative

species abundance), we used canonical analyses of

principal coordinates, CAP (Anderson and Willis

2003), and multivariate regression trees, MRT (De’ath

2002). CAP was used to examine patterns of community

differences between locations as well as between

treatments at each location. CAP is a constrained

ordination technique that further analyzes the results

of a principal coordinates analysis (PCO), for which the

type of ecological distance can be chosen. It enables

testing of significant grouping structure within the

ordination by using permutation tests to assign a P

value to the a priori hypothesis that the probability of

the grouping found in the analysis could be due to

chance alone by ‘‘leave-one-out’’ allocations. MRTs

were then conducted to test the differences and

similarities between groups. This multivariate discrimi-

nation technique constructs a hierarchical tree by

creating splits, which minimize the dissimilarity of

groups within clusters. Both CAP and MRT analyseswere based on the Bray-Curtis dissimilarity measure of

log-transformed abundance data (ln (x þ 1)) of the fishon each replicate reef during the last survey. Lognormal

transformations were applied to reduce the emphasis ofhighly abundant species, which would otherwise drivemost of the observed patterns, and Bray-Curtis distances

are generally considered well suited for abundance data.Recruitment of apogonids (cardinalfish) was very high

at Lizard Island, with many reefs receiving hundreds ofindividuals. Because this group of fish is known to

influence patterns in fish communities, apogonid specieswere excluded from CAP and MRT analyses to enable

differences in the majority of fish species betweentreatments to be detected. Rare species (fewer than five

individuals sighted over 12 months) were also excluded.The number of permutations in the CAP analyses was

set to 100. The default was selected for the number ofmeaningful PCO axes (m), which chooses the optimal

number of axes in order to provide the best distinctionbetween groups and maximizes the proportion of correct

allocations to the grouping variable and minimizesmisclassification error (Anderson and Willis 2003). The

first two axes, which explained most of the variation,were illustrated in an ordination plot. Dispersion ellipsesusing 0.9 confidence limits of the standard deviation of

point scores were also plotted. Species showing thestrongest indication of difference between treatments

(i.e., correlation with axis 1 and/or axis 2 . 0.2) wereplotted separately and listed in the Appendix: Table A1.

In the MRT analyses, the best tree size was chosen bycross-validation and the 1 SE rule. The relative error

corresponds to the amount of variation among samplesnot explained by the tree (De’ath 2002). All analyses and

plots were coded in R 2.10.0 (R Development CoreTeam 2009) using the R statistical packages vegan,

BiodiversityR, MASS, and mvpart.

RESULTS

Regional difference in local species composition

In total, 150 fish species colonized the patch reefs atLizard Island and 122 species were recorded in Kimbe

Bay. Of the overall total of 219 fish species, 53 (24.2%)were observed at both locations, representing ;35% of

the Lizard Island fish community and ;43% of theKimbe Bay community. The composition of fish

communities was very different between the twolocations (Appendix: Fig. A2).

Effects of coral species richness on fish species richness,evenness, and abundance

Fish species richness significantly increased with

increasing coral species richness in Kimbe Bay, withthe single-coral treatments supporting significantlylower fish species richness (13.6 fish species) than the

medium- (17.7 fish species) and high- (20.0 fish species)diversity coral treatments (Fig. 1B, Table 2A). At Lizard

VANESSA MESSMER ET AL.2288 Ecology, Vol. 92, No. 12

Island, mean fish species richness increased from 21.0 to

25.0 species with increasing coral species richness, but

here the difference was not statistically significant (Fig.

1A, Table 2A). Evenness of the fish communities did not

differ among different levels of coral species richness at

either location (Fig. 1C, D, Table 2A).

No significant differences in mean total fish abun-

dance were observed between different levels of coral

species richness (Fig. 1E, F, Table 2A). Pooled mean

abundances of fish were higher at Lizard Island (273.7 6

28.7 fish, mean 6 SE) than in Kimbe Bay (120.0 6 29.2

fish; ANOVA: F1,88 ¼ 24.75, P , 0.001), which was

primarily driven by the presence of large schools of

apogonids at Lizard Island. Distributions of Chromis

viridis (a damselfish) were patchy, as this species was

either absent or occurred in large schools. Pooled mean

fish abundances not including apogonids and C. viridis

were more similar between both locations, although still

significantly higher at Lizard Island than in Kimbe Bay

(81.2 6 4.3 fish and 60.8 6 4.3 fish, respectively;

ANOVA: F1,88¼ 12.16, P , 0.001). There was no effect

of coral species richness on abundance when apogonids

and C. viridis were excluded from analysis (Fig. 1G, H,

Table 2A).

FIG. 1. Effects of three levels of coral species richness (low¼ 1, medium¼ 3, high¼ 6 species) on fish communities of LizardIsland (Great Barrier Reef, Australia) and Kimbe Bay (Papua, New Guinea): (A, B) fish species richness (all species); (C, D)Shannon evenness index (all species); (E, F) total fish abundance per patch reef, ;1 m2 (all species); and (G, H) fish abundance perpatch reef, not including apogonids (cardinalfish) or Chromis viridis (a damselfish). Values are shown as mean 6 SE; see Table 2A.Lowercase letters (panel B) indicate significant differences (P , 0.05) identified by Tukey’s hsd post hoc tests.

December 2011 2289CORAL REEF HABITAT AND FISH DIVERSITY

Effects of coral species composition on fish species

richness, evenness, and abundance

Fish species richness differed between treatments at

both locations (Fig. 2A, B, Table 2B). The high-diversity

(H) and medium B-diversity (MB) treatments supported

the highest number of fish species in both locations.

However, some single-coral treatments (An and Sh)

supported similarly high fish species richness (Fig.

2A, B, Table 2B), and these coral types probably

contributed to the high species richness seen in the

combination treatments medium B and high. In

contrast, other coral species tended to support low

species richness at one (e.g., Bb and Pd in Kimbe) or

both locations (e.g., Pc and St), of which Pc, Bb, and Pd

form the medium A treatment, where similarly low fish

species richness was observed. Evenness was similar

across treatments at Lizard Island, with no significant

differences between treatments (Fig. 2C, Table 2B), but

it differed statistically among treatments in Kimbe Bay

(Fig. 2D, Table 2B). Low evenness in the An and

medium B treatments was driven by the presence of

large schools of Chromis viridis on some replicates.

Removal of C. viridis from the analysis caused evenness

to be similar across most treatments, with only Pd

showing significantly lower values than Pc (P ¼ 0.010).

In contrast to the low abundances and species richness

observed in the treatments St and Pc, values of evenness

were among the highest in these corals. Total fish

abundance, including all fish species per reef, did not

differ between treatments at Lizard Island (Fig. 2E,

Table 2B), whereas in Kimbe Bay, total abundances

were found to be markedly higher on patch reefs of the

treatments An and medium B (Fig. 2F, Table 2B). The

high variation in abundance of some treatments at both

sites was largely driven by large schools of Chromis

viridis, which were found on three of the six coral species

at Lizard Island (Acropora nasuta, Pocillopora damicor-

nis, Seriatopora hystrix), but on just one in Kimbe Bay

(A. nasuta). When apogonids and C. viridis were

excluded from the analyses, mean abundances at Lizard

Island were significantly lower in the Pc and St

treatments than in Bb, Pd, and Sh (Fig. 2G, Table

2B). In Kimbe Bay, mean fish abundances were also

significantly lower in Pc and St than in An, Bb, Pd, and

medium B (Fig. 2H, Table 2B).

Effects of coral species on composition of fish community

Clear differences in the composition of fish communi-

ties between treatments were observed for both locations.

TABLE 2. For Lizard Island (LI) and Kimbe Bay (KB), one-way ANOVA testing the effects of (A) coral species richness and (B)reef treatment on fish species richness, Shannon evenness index, total fish abundance, and fish abundance excluding apogonids(cardinalfish) and Chromis viridis (a damselfish).

Effect SS effect df effect SS residuals df residuals F P

A) Coral richness

Fish species richness

LI 73.9 2 876.4 42 1.77 0.183KB 254.5 2 619.3 42 8.63 ,0.001

Fish evenness

LI 0.0 2 0.3 42 1.98 0.150KB 0.1 2 1.7 42 0.84 0.438

Total fish abundance

LI 33 757 2 812 250 42 0.87 0.425KB 15 689 2 1 027 759 42 0.32 0.728

Fish abundance excluding two taxa

LI 318 2 35 929 42 0.19 0.831KB 415 2 36 976 42 0.24 0.791

B) Reef treatment

Fish species richness

LI 503.1 8 447.2 36 5.06 ,0.001KB 517.0 8 356.8 36 6.52 ,0.001

Fish evenness

LI 0.0 8 0.3 36 0.72 0.674KB 0.9 8 0.9 36 4.50 ,0.001

Total fish abundance

LI 106 774 8 739 233 36 0.65 0.731KB 502 680 8 540 768 36 4.18 0.001

Fish abundance excluding two taxa

LI 16 701 8 19 547 36 3.84 0.002KB 21 217 8 16 173 36 5.90 ,0.001

Notes: The Shannon evenness index was arcsine square-root transformed. Effects of coral richness (1, 3, and 6 species) are shownin Fig. 1. Coral reef treatments were low-diversity (single coral species An, Bb, St, Pc, Pd, Sh); medium A and medium B (twogroups of three species); and high (six coral species). Effects are shown in Fig. 2.

VANESSA MESSMER ET AL.2290 Ecology, Vol. 92, No. 12

At Lizard Island, fish communities inhabiting each coral

species were quite distinct; the six single-species treat-

ments (An, Bb, Pc, Pd, Sh, and St) formed clusters in the

ordination graph with little overlap (Fig. 3A). In contrast,

fish communities on the treatments of higher coral species

richness seemed to represent a mixture of those found on

each of its constituent coral species; their clusters

overlapped with their constituent single-species treat-

FIG. 2. Effects of coral species composition on fish communities of Lizard Island and Kimbe Bay for each treatment: (A, B) fishspecies richness (all species); (C, D) Shannon evenness index (all species); (E, F) total fish abundance (all species); and (G, H) fishabundance excluding apogonids and Chromis viridis. These two taxa were excluded because of their patchy occurrence due to highrecruitment on some reefs and schooling behavior. Values are shown as means 6 SE (see Table 2B). Lowercase letters indicatesignificant differences (P , 0.05) identified by Tukey’s hsd post hoc tests. Treatment patch reefs were low diversity (single coralspecies: An, Bb, Pd, Sh, St), medium diversity (two combinations of three different coral species each: MA, MB), or high diversity(six coral species: H); see Table 1 for full scientific names.

December 2011 2291CORAL REEF HABITAT AND FISH DIVERSITY

ments. For example, medium A overlapped largely with

Bb, whereas An and Sh are both constituents of medium

B, which was embedded within their cluster. The high-

diversity treatment was located in the middle of the plot,

overlapping with most treatments.

The distinction between fish communities of different

treatments using CAP was even stronger in Kimbe Bay

(Fig. 4A). Similarities between fish communities on the

high-diversity coral species richness treatments and

those of their constituent coral species were also

observed there. Medium A slightly overlapped with

Pd, which constitutes one of its species. The An cluster

overlapped to some degree with medium B and the Sh

cluster was situated in close proximity. High coral

species richness appeared to promote a mixture of the

fish communities found on the constituent coral species,

as suggested by the relatively central location of the

high-diversity treatment and dispersed spread of this

cluster in the ordination plot.

At Lizard Island, many fish species preferred partic-

ular coral species; 66% of the species used in the analysis

were strongly correlated (.0.2) with one or both CAP

axes (Fig. 3B; also see the Appendix: Table A1). The

differences between fish communities on different coral

species were driven by a variety of fish species covering a

range of reef fish families, but consisted in particular of

gobies, damselfishes, and butterflyfishes (Fig. 3B;

Appendix: Table A1). Many of these species preferred

An, Sh, and Pd over other corals (V. Messmer,

unpublished data). Very similar patterns were observed

in Kimbe Bay, where 62% of the species were strongly

correlated with one or both of the CAP axes (Fig. 4B;

Appendix: Table A1). A considerable proportion of the

species driving the differences in fish communities

between treatments was also accounted for by gobies,

whereas only a few damselfish species showed a

preference for particular coral species. In contrast to

Lizard Island, only a few species preferred Pd and the

distinction of the fish community on St seemed to be

largely driven by the absence or low abundances of

many species, as no fish species preferred this coral

species (Fig. 4B; Appendix: Table A1).

The distinction between fish communities from

different coral species at Lizard Island found in the

CAP analysis was supported by the MRT, with 46.8% of

the total variation explained by the treatments (Fig. 3C).

The MRT provided information on similarities/dissim-

ilarities among the fish assemblages. Those on Pc and St

were most different from all others, as they formed the

first split of the tree, explaining most of the variation

between groups. The second split based on the

remaining variation separated Pd and medium A, with

Pd being part of medium A. Next, An split from the

remaining treatments and the final split distinguished Pd

from the cluster Sh, medium B, and H, Sh being part of

medium B. Very similar results were also found for

Kimbe Bay, equally supporting the CAP analysis (Fig.

4C). The treatments explained 46.8% of the total

variation. Pc, St, and Bb formed the first split, with fish

assemblages on St and Pc being more similar. These

three treatments were most distinct from all other

treatments, explaining most of the variation. The first

split within the other major branch of the tree separated

Pd with medium A and H, with Pd being part of medium

A. Of the remaining treatments, Sh split from the cluster

An and medium B, with An being part of medium B.

DISCUSSION

Through experimentally minimizing the effects of

environmental variables, our results directly demon-

strated the importance of microhabitat (coral) species

richness and composition to the local species richness,

composition, and abundance of reef fish communities.

The component of fish diversity that was most affected

by the experimentally imposed variation in habitat was

species richness. Coral species richness promoted local

fish species richness, tended to increase fish evenness, but

had little effect on the overall abundance of fishes.

Furthermore, different microhabitats were found to

strongly influence the structure of the associated animal

communities. Certain coral species supported signifi-

cantly more abundant and diverse fish assemblages than

others, but had little effect on evenness, suggesting that

habitat diversity and composition do not necessarily

influence the relationship between fish species richness

and fish abundance. There were also substantial

differences in the composition of fish communities

associated with different coral species, and a habitat

patch composed of several coral species supported a fish

assemblage that reflected the particular composition of

microhabitat (coral) types. These results were remark-

ably consistent between the two geographic locations,

despite having ,25% of fish species in common. The

consistency in the response of fish communities to coral

identity and species richness, regardless of differences in

regional species composition or other environmental

!FIG. 3. Lizard Island, December 2008. (A) Canonical analysis of principal coordinates (CAP) ordination plot (Bray-Curtis) of

fish assemblage data showing treatment effects; each point represents a separate patch reef. CAP groupings were stronglysupported, with 66.7% correct allocations (P ¼ 0.001). Six PCO axes produced the best result, accounting for 68.0% of the totalvariation. PCO axes 1 and 2 explained 22.8% and 12.9% of the total variation, respectively. (B) Species scores for CAP plots and(C) multivariate regression tree (MRT) based on a Bray-Curtis dissimilarity matrix of log-transformed fish abundance data, usingtreatments as groupings. In panel (B), letter-number codes are provided for each fish species showing correlations of r � 0.20 witheither canonical axis (C, chaetodontids; L, labrids; P, pomacentrids; G, gobies; O, other fish groups). Species names and r values arespecified in Appendix A: Table A1.

VANESSA MESSMER ET AL.2292 Ecology, Vol. 92, No. 12

December 2011 2293CORAL REEF HABITAT AND FISH DIVERSITY

features, highlights the importance of diversity in

habitat-forming species in promoting and maintaining

local fish diversity on coral reefs.

Using correlative data, positive relationships between

coral and fish diversity have also been found at small

(Luckhurst and Luckhurst 1978, Bell and Galzin 1984,

Roberts and Ormond 1987, Ohman and Rajasuriya

1998, Komyakova 2009) and large spatial scales

(Hughes et al. 2002, Bellwood and Meyer 2009), yet

the relationship had never been experimentally verified

for coral reefs. Such positive correlations in species

richness between taxa are commonly observed across

ecosystems (Lawton 1983, Currie 1991, Tews et al. 2004,

Wolters et al. 2006, Jetz et al. 2009), but the underlying

processes are still poorly understood (Rahbek and

Graves 2001). Although habitat diversity has long been

recognized as a potential driver of animal diversity

(‘‘producer–consumer hypothesis’’ and ‘‘habitat struc-

ture hypothesis’’) (Hutchinson 1959), climate and other

environmental variables (e.g., energy) also are often

invoked in a third hypothesis as principal factors

producing positive relationships (Hawkins and Porter

2003). Few attempts have been made to disentangle the

relative roles of these underlying processes and the

results are not always consistent. No positive effects of

habitat diversity on the diversity of associated animals

have been found in some correlative studies after

environmental variables were accounted for (Hawkins

and Porter 2003, Jetz et al. 2009), whereas in others the

contribution of habitat diversity was strong (Kerr and

Packer 1997, Marquez et al. 2004, Novotny et al. 2006,

Kissling et al. 2007, Menendez et al. 2007, Kissling et al.

2008, Hortal et al. 2009, Qian et al. 2009). The

advantage of experimental studies is that the influence

of environmental variables can be minimized, which

allows for direct testing of the importance of habitat

diversity itself. We are only aware of two such studies,

both conducted in terrestrial systems: in each of them,

plant species richness positively affected the species

richness of insects (Siemann et al. 1998, Haddad et al.

2001). The positive relationship between coral and fish

species richness found here supports these findings and

suggests that direct positive effects of habitat diversity

can also play an important role in the marine

environment. Although environmental variables (hy-

pothesis three) are also likely to play an important role

in general, particularly at large spatial scales, they did

not contribute to the positive effects of coral diversity on

fish diversity observed here. Instead, our results indicate

that the ‘‘producer–consumer hypothesis’’ and/or the

‘‘habitat structure hypothesis’’ clearly influence local

patterns of fish and coral diversity. To what degree

habitat diversity may work synergistically with other

proposed processes (Bellwood and Wainwright 2002,

Mora and Robertson 2005) in producing known

congruent species patterns among coral reef organisms

at very large spatial scales is yet to be tested.

The positive influence of plant species richness on the

diversity of associated animal communities, in particular

that of specialist herbivores, has often been attributed to

the availability of a greater diversity of resources, which

are thought to provide opportunities for niche parti-

tioning and the coexistence of species (Hutchinson 1959,

Murdoch et al. 1972, Chesson 2000, Novotny et al. 2006,

Kissling et al. 2007). Processes of habitat selection and

resource specialization are well known in the terrestrial

environment and play a fundamental role in structuring

ecological communities (Futuyma and Moreno 1988,

Morris 2003). Resource partitioning can occur either in

food resources (producer–consumer hypothesis)

(Hutchinson 1959, Chesson 2000, Novotny et al. 2006)

or in the provision of habitat (habitat structure

hypothesis) (Tews et al. 2004). These patterns of

habitat–animal associations also appear to apply to

coral reef systems. Like plants, corals provide both food

and habitat in which associated communities reside. On

coral reefs, strong, even obligate, associations occur

between reef fish species and certain corals (Munday et

al. 1997, Pratchett 2005), although less specialized

species also often exhibit some level of preference for

certain coral species (Munday et al. 1997, Gardiner and

Jones 2005, Cole et al. 2008, Wilson et al. 2008).

The concept of niche partitioning as a driving

mechanism for positive habitat–animal relationships is

supported by our results, as clear patterns of habitat

selection by fish species among the six coral species

investigated were confirmed by the multivariate analy-

ses. However, other post-settlement processes, such as

predation, cannot be excluded. Nearly two-thirds of the

species at both locations were strongly associated with

microhabitats, suggesting that habitat selection is

deterministic in structuring fish communities on coral

reefs. Clear choices for a particular coral species as food

or shelter, in particular Acropora nasuta, Seriatopora

hystrix, and Pocillopora damicornis, were often observed

in highly specialized fishes. Habitat selection in coral-

feeding fishes, e.g., butterflyfishes (Chaetodon spp.)

(Pratchett and Berumen 2008), supported the ‘‘produc-

er–consumer hypothesis.’’ However, the ‘‘habitat struc-

ture hypothesis’’ best explained our results, as the

!FIG. 4. Kimbe Bay, November 2007. (A) Canonical analysis of principal coordinates (CAP) ordination plot (Bray-Curtis) of

fish assemblage data showing treatment effects; each point represents a separate patch reef. Groupings were strongly supported,with 93.3% correct allocations (P¼ 0.001). The best result consisted of 13 principal coordinates axes, accounting for 96.1% of thevariation. Axes 1 and 2 explained 19.7% and 14.1% of the variation, respectively. (B) Species scores for CAP plots and (C)multivariate regression tree (MRT) constructed on a Bray-Curtis dissimilarity matrix of log-transformed fish abundance data,using treatments as groupings. Codes are as in Fig. 3.

VANESSA MESSMER ET AL.2294 Ecology, Vol. 92, No. 12

December 2011 2295CORAL REEF HABITAT AND FISH DIVERSITY

majority of species displaying habitat preferences

selected particular coral species for living space and

shelter, e.g., coral-dwelling gobies (Munday 2000), but

so did less specialized planktivorous pomacentrids. By

contrast, staghorn Acropora and Porites cylindrica

seemed to be actively avoided by a number of reef

fishes, whereas other fish species were found exclusively

on these corals. Not surprisingly, and consistent with the

concept that particular organisms are associated with

particular microhabitats (Bernays and Graham 1988),

the patch reefs characterized by higher coral species

richness supported fish communities that represented a

mixture of those found on the constituent coral species.

Although habitats characterized by higher coral diver-

sity did not necessarily support more diverse or

abundant fish communities than did some single-coral-

species patches, a diverse habitat contains more micro-

habitats that are likely to be preferred or strongly

selected for by a significant number of different coral

reef fishes and should result in overall higher animal

diversity.

In addition to better understanding the processes

producing positive relationships between habitat and

animal diversity, our results also highlight the critical

importance of particular components of the habitat (in

this case, individual coral species) in establishing this

relationship. The relationship was strikingly dependent

on the particular corals included in the diversity

treatments, suggesting that particular coral species,

and not necessarily coral diversity per se, are critical

for sustaining diverse and abundant fish communities.

Variation in fish diversity and community structure

between coral species is not unexpected, as coral species

vary in morphology and many fish species preferentially

associate with certain coral species (Hixon and Menge

1991, Munday et al. 1997, Holbrook et al. 2002). In our

experiment, Porites cylindrica and staghorn Acropora

were characterized by consistently low fish species

richness. In Kimbe Bay, bottlebrush Acropora, and

Pocillopora damicornis, which together with Porites

cylindrica formed the medium A treatment, displayed

similarly low fish species richness, and this was mirrored

by low fish species richness in the medium A treatment.

In contrast, fish species richness of the medium B

treatment was equal to the high-diversity treatment

because they both shared coral species that supported

high fish species richness, in particular Acropora nasuta

and Seriatopora hystrix. The discrepancy in diversity

between the medium diversity treatments thus is likely to

reflect the ‘‘performance’’ of their constituent coral

species in terms of fish species richness. Differences in

the ‘‘performance’’ of corals were also reflected in

patterns of total fish abundance, which were little

affected by coral species richness, but varied significantly

with coral identity and composition. Patterns of mean

abundance (not including apogonids and Chromis

viridis) were strikingly similar between locations and,

importantly, also mirrored patterns of fish species

richness. Coral identity played an important role in

maintaining abundant fish communities, with Porites

cylindrica and staghorn Acropora consistently support-

ing the lowest fish abundances. This may have been due

to the more open branching structure of these corals

compared to the other coral species, potentially provid-

ing less appropriate shelter relative to the size of the

patch reefs. At both sites, mean fish abundances were

high in the treatments of higher coral species richness,

but not more so than particular coral species, such as

Acropora nasuta, bottlebrush Acropora, Pocillopora

damicornis, and Seriatopora hystrix.

Differences in the capacity of different coral species to

promote and maintain abundant and diverse fish

communities is of great concern, because the health of

coral reefs is declining at a global scale (Hoegh-

Guldberg 1999, McClanahan 2002, Gardner et al.

2003, Wilkinson 2004) and increasing numbers of coral

species are expected to undergo reductions in abun-

dance, at least at local scales. The clear preference of

many fish species for particular types of coral suggest

that certain microhabitats, such as Acropora nasuta and

Seriatopora hystrix, play a particularly important role in

promoting diverse local fish communities, but these

particular coral species are also known to be highly

susceptible to disturbances (Marshall and Baird 2000,

Loya et al. 2001, McClanahan et al. 2007). Loss of these

species could have a disproportionately strong impact

on local fish communities. Similarly, Tews et al. (2004)

reviewed a number of studies that identified crucial

keystone structures in the vegetation to which different

species groups were closely linked and that dispropor-

tionately influenced animal species. A shift in the habitat

community structure therefore has the potential to result

in less diverse and abundant animal communities and

significant alterations in their composition.

The remarkable congruence in the response of fish

communities to coral diversity and identity between the

two locations highlights the strength and nature of the

relationship between fish and corals. The effects of coral

diversity and identity on fish composition, diversity, and

abundance were similar, despite the differences in the

fish communities and overall higher fish diversity and

abundance observed at Lizard Island. The use of a field

experiment enabled us to investigate for the first time the

specific influence of specific coral species and coral

diversity on the structure of coral reef fish communities,

the nature of the relationship between coral diversity

and fish diversity, and the potential consequences of

declines in coral diversity. A direct causal link between

local coral and fish diversity has been established, which

was best explained by habitat selection for shelter, but in

some cases also for food. Our results also highlighted the

variable contributions that different species of corals

make in maintaining patterns of species richness and

community structure of the associated fish assemblages.

Although many coral reef fish may be able to use a

number of microhabitats, selective preference for specific

VANESSA MESSMER ET AL.2296 Ecology, Vol. 92, No. 12

coral species by some species was clearly evident in our

study. The overall potential for a strong, positive

relationship between coral diversity and fish diversity

has the consequence that ongoing degradation of coral

reefs worldwide will probably greatly alter the diversity

and structure of associated fish communities, in partic-

ular due to the loss of specialized species with distinct

resource requirements.

ACKNOWLEDGMENTS

We thank the Lizard Island Research Station (LIRS),Mahonia Na Dari, and the Moorea Coral Reef LTER forlogistical support; K. Chong-Seng, S. Tang Smith, J. Johans-son, P. Saenz Agudelo, M.-E. Portwood, K. Markey, N.Crawley, G. Vima, and M. Giru for assistance in the field; andJ. Claudet for statistical help. Funding was provided by an IanPotter Foundation Fellowship at LIRS and Graduate ResearchScheme (JCU) to V. Messmer; ARC Centre of Excellence forCoral Reef Studies funding to G. P. Jones, and PLM and USANSF funding to R. J. Schmitt, S. J. Holbrook, and A. J.Brooks. This work was carried out under James CookUniversity Ethics Approval No. A1207. Comments fromanonymous reviewers greatly improved the manuscript.

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APPENDIX

Additional figures and tables, including a map showing study locations, a CAP analysis demonstrating differences in fishcommunities between locations, and the species lists for Figs. 3B and 4B (Ecological Archives E092-198-A1).

VANESSA MESSMER ET AL.2298 Ecology, Vol. 92, No. 12