Coral Reefs (2008) 27:97–104

DOI 10.1007/s00338-007-0294-y

REPORT

Nocturnal relocation of adult and juvenile coral reef Wshes in response to reef noise

S. D. Simpson · A. JeVs · J. C. Montgomery · R. D. McCauley · M. G. Meekan

Received: 2 February 2007 / Accepted: 8 August 2007 / Published online: 1 September 2007© Springer-Verlag 2007

Abstract Juvenile and adult reef Wshes often undergomigration, ontogenic habitat shifts, and nocturnal foragingmovements. The orientation cues used for these behavioursare largely unknown. In this study, the use of sound as anorientation cue guiding the nocturnal movements of adultand juvenile reef Wshes at Lizard Island, Great Barrier Reefwas examined. The Wrst experiment compared the move-ments of Wshes to small patch reefs where reef noise wasbroadcast, with those to silent reefs. No signiWcant responseswere found in the 79 adults that were collected, but the 166juveniles collected showed an increased diversity eachmorning on the reefs with broadcast noise, and signiWcantlygreater numbers of juveniles from three taxa (Apogonidae,Gobiidae and Pinguipedidae) were collected from reefswith broadcast noise. The second experiment compared themovement of adult and juvenile Wshes to reefs broadcastinghigh (>570 Hz), or low (<570 Hz) frequency reef noise, or

to silent reefs. Of the 122 adults collected, the highestdiversity was seen at the low frequency reefs; and adultsfrom two families (Gobiidae and Blenniidae) preferredthese reefs. A similar trend was observed in the 372 juve-niles collected, with higher diversity at the reefs with lowfrequency noises. This preference was seen in the juvenileapogonids; however, juvenile gobiids were attracted to bothhigh and low sound treatments equally, and juvenile stageAcanthuridae preferred the high frequency noises. This evi-dence that juvenile and adult reef Wshes orientate withrespect to the soundscape raises important issues for man-agement, conservation and the protection of sound cuesused in natural behaviour.

Keywords Post-settlement migration · Coral reef Wshes · Reef noise · Nocturnal movement · Orientation · Patch reefs

Introduction

Juvenile and adult reef Wshes often undergo nocturnalforaging movements, ontogenetic habitat shifts, andmigrations. At small scales (m–100 m), site-attached adultcardinalWshes (family Apogonidae) can navigate success-fully across reef habitat to feed at night, returning to sheltersites before sunrise (Marnane 2000; Kolm et al. 2005).Ontogenetic migrations can take place at slightly largerscales (m–km), where reef Wshes settle into nursery areas,rather than directly into adult habitats. For example, sea-grass beds are known to be important nursery grounds(Pollard 1984; Beck et al. 2001) from which Wshes laterundergo ontogenic migrations to adjacent coral reef habitat(Shulman and Ogden 1987; Nagelkerken et al. 2000). Atlarger spatial scales, adult reef Wshes (e.g., Acanthuridae,Serranidae, Lethrinidae and Lutjanidae) may migrate tens

Communicated by Biology Editor M. P. Lesser.

S. D. Simpson (&)Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Kings Buildings, Edinburgh EH9 3JT, UKe-mail: s.simpson@ed.ac.uk; simpsonstephen@hotmail.com

A. JeVs · J. C. MontgomeryLeigh Marine Laboratory and School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

R. D. McCauleyCentre for Marine Science and Technology, Curtin University, GPO Box U 1987, Perth 6845, Australia

M. G. MeekanAustralian Institute of Marine Science, PO Box 40197, Casuarina, Darwin, NT 8010, Australia

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to hundreds of km to speciWc and traditional spawning sites(Colin and Clavijo 1988; Warner 1988; Domeier and Colin1997).

The sensory cues that guide these movement patternsare largely unknown and are likely to vary amongst spe-cies, between habitats, and with time of day (Montgomeryet al. 2001; Kingsford et al. 2002). For example, visualcues can be important during daylight, so that when theposition of landmarks on natural patrol routes are manipulated,butterXyWshes (family Chaetodontidae) may spend timesearching for displaced landmarks (Reese 1989) whilesurgeonWshes (family Acanthuridae) may alter their originalpaths according to new landmark positions (Mazeroll andMontgomery 1998). At night, however, visual cues are ofless value and chemical and acoustic cues may be ofprimary importance.

Reef noise produces a large-scale “cuescape” which isunaVected by local water movement (unlike chemicalcues), since sounds propagate in water with little attenua-tion and irrespective of current (Rogers and Cox 1988).Furthermore, coral reefs produce unusually high levels ofbiological sound within the hearing range of most Wshes(Cato 1978), especially at night when movements may begreatest to avoid visual predators. Reef noise typically con-sists of a constant “crackle” produced by the simultaneoussnaps of multiple snapping shrimps (peak-to-peak sourcelevel 189 dB re 1 �Pa at 1 m (Au and Banks 1998), soundgenerated by imploding bubbles at the claw-tips (Versluiset al. 2000)). In addition, Wsh produce noises at source lev-els up to 157 dB re 1 �Pa at 1 m, which include pops (5–28 ms), whoops (2–4 ms) and grunting sounds (Cato 1980;McCauley and Cato 2000), and the chorus of nocturnalWshes can raise the sound proWle of a reef by 35 dB re 1 �Paabove background levels (McCauley and Cato 2000). It isprobable that this biological noise is indicative of the sur-rounding fauna, potentially facilitating habitat selection.

Given the ubiquity of underwater sound, the physicalproperties that enhance its availability as a cue, and the factthat acoustic cues are known to be utilised by settlement-stage coral reef Wshes to locate and orient to suitable settle-ment sites (Simpson et al. 2005; Montgomery et al. 2006),it seems highly likely that adult and juvenile reef Wshes mayalso use sound as a orientation cue. To date, no study hasinvestigated the eVect that reef noise may have on thebehaviour of juvenile and adult Wshes, and its potential forattracting these Wshes to speciWc habitats. In this study, aseries of experimental patch reefs on open sand Xats wereused to monitor the arrival of juvenile and adult reef Wshesresulting from nocturnal movements in response to noise.Full spectrum and high and low frequency Wltered record-ings of natural reefs were used to compare the movement ofWsh with respect to the presence or absence of diVerentnoise treatments.

Materials and methods

This study was carried out in the nearshore waters of LizardIsland Research Station, Great Barrier Reef during the newmoon periods of November and December 2003. In theNovember study (Experiment 1), a full spectrum recordingof reef noise was broadcast at some patch reefs, while oth-ers received no broadcast noise. In the December study(Experiment 2), high frequency and low frequency Wlteredrecordings of reef noise were broadcast at some reefs, whileothers received no broadcast noise. In Experiment 1, foursites (separated by at least 300 m) were selected using acombination of satellite images, charts, and SCUBA sur-veys to ensure they were located at least 250 m from thenearest established reef (A–D, Fig. 1). At each site, twomoorings were deployed (separated by at least 100 m) con-sisting of a concrete block with rope (chain was not used toavoid clinking), and a polystyrene Xoat. Three patch reefs(0.1 m3 each) consisting of coral rubble collected from theedges of live reefs in the same area were built 5 m fromeach mooring in a triangular formation (Fig. 1). This meantthat for Experiment 1, there were four replicate sites; eachwith a pair of moorings that had three reefs each. In Experi-ment 2, two sites were used (A and D), and each had threemoorings (separated by at least 100 m), which had fourreefs each (Fig. 1).

The same recording of reef noise that had attracted set-tlement-stage coral reef Wshes in previous studies (Simpsonet al. 2004, 2005) was used in this study. It consists of afour-minute looped section played throughout the nighttaken from a recording of the dusk chorus of biologicalnoise recorded during the time of the new moon, and ismade up of a chorus of pops made by nocturnal Wshestogether with a higher frequency (2.5–200+ kHz) but lowerintensity background crackle produced by snappingshrimps as well as other feeding, movement, and callingsounds.

Experiment 1: Reef noise vs. silent

Experiment 1 was conducted over six nights centred on theNovember new moon, with six consecutive nights of sam-pling at sites A and B, and Wve nights of sampling at sites Cand D (the delay at C and D was due to the logistics ofmoving and constructing the 12 reefs which took 2 days).Sound systems broadcasting full sound spectrum reef noisewere attached to one in each of four pairs of moorings(Fig. 2). The sound systems consisted of a marine battery,CD player and ampliWer housed in a Xoating barrel towhich an underwater speaker (Lubell Labs Inc., Columbus,OH; LL964, frequency response 0.2–20 kHz, broadbandsource level set at 156 dB re 1 �Pa at 1 m) was suspended2 m underneath. It was predicted that at this source pressure

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level, using diVerent models of sound propagation, theintensity would be between 139 (spherical model) and 147(cylindrical model) dB re 1 �Pa at the reefs themselves.Although there were no facilities to measure backgroundambient noise during this study, the output can be com-pared to measurements made in the same location during an

earlier study (Tolimieri et al. 2004). Daytime measure-ments of a similar signal, broadcast at 180 dB re 1 �Pa at1 m, were found to be 20 dB above ambient noise levels at80 m from the speaker. Using two models of sound propa-gation, predictions of the received level range between 142(spherical) and 162 (cylindrical) dB re 1 �Pa at 80 m,which, if 20 dB above ambient, puts the daytime ambientnoise in the range 122–142 dB re 1 �Pa in the study area.Since the nocturnal chorus can raise the sound proWleby 35 dB above background levels (McCauley and Cato2000), potentially raising the predicted ambient noise to alevel of 157–177 dB re 1 �Pa, the broadcast levels in thisstudy (156 dB re 1 �Pa at 1 m) appear appropriate, and pos-sibly conservative. The allocation of the sound system wasalternated each night within a pair. To the silent mooring ineach pair (although this treatment is called “silent”, therewas obviously some ambient noise) a dummy barrel andspeaker of equal dimensions was attached to control for anyattraction of reef Wshes to these Xoating objects.

Each morning divers collected the juvenile and adult Wsh(as well as settled larvae; reported in Simpson et al. 2005)from each reef using clove oil and hand nets. The Wsh were

Fig. 1 Location of study site at Lizard Island, showing the research station and adjoining sandy bay in which experimental patch reefs were constructed. In Experiment 1 (November), two sets of three reefs were con-structed at locations A–D, whereas in Experiment 2 (December), three sets of four reefs were constructed at loca-tions A and D

November Sound-Silent

A

B C

D

December High-Low-Silent

silent

sound Sound system

Patch reef

High freq.

Low freq. Silent

Fig. 2 Experimental apparatus showing conWguration of the reefs andunderwater sound playback equipment. Replicate reefs were 100 mapart, and constructed in 3–6 m depth on a sandy seabed. Drawing notto scale

>100 m

permanent mooring

3-6 m depth

surface buoy

dummy rig

dummyspeaker

sound system

speaker broadcasting

reef noise

patchreefs

a b

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preserved in alcohol immediately after capture, and trans-ferred to the laboratory where they were identiWed andcounted.

Experiment 2: High frequency vs. low frequency reef noise vs. silent

Experiment 2 was conducted over eight nights centred onthe December new moon, with eight consecutive nights atsite D and seven nights at site A (the delay at A was due tothe logistics of moving 12 reefs which again took 2 days).Two sound systems (as above) and a dummy rig were dis-tributed randomly within each of two sets of three mooringseach night. One sound system broadcast high frequencyWltered reef noise (Bandpass Wlter, 500–2,000 Hz, resultingin 80% of actual broadcast noise energy > 570 Hz, Fig. 3),while the other broadcast low frequency noise (BandpassWlter 20–500 Hz, resulting in 80% of actual broadcast noiseenergy < 570 Hz); the dummy system produced no noise.Sound system output was balanced so that equal soundenergy (156 dB re 1 �Pa at 1 m) was broadcast by each sys-tem. Fish were collected from the reefs each morning.

Statistical analysis

Due to low and variable numbers of Wshes collected eachnight, taxa were grouped and analysed at the family level,except for the analysis of diversity per night, which wasconducted both at the family and species level. First, toinvestigate the Wnal ratio of individuals collected by eachtreatment, a Chi-squared (�2) test was used, testing the nullhypothesis (H0) that the catches would be split equallybetween treatments (Zar 1999). This test assumes that therewas equal sampling eVort for each treatment, and assumesthat each Wsh is an individual (i.e., Wsh do not arrive ingroups).

Second, to compare catches between treatments for eachsite on each night, the Wilcoxon’s Signed Rank test wasused for data sets from Experiment 1 and the Friedman’stest was used for data from Experiment 2. The catches forreefs at each mooring were pooled to increase sample size.These nonparametric methods test the H0 that paired orrelated variables (by site and date) have the same distribu-tion despite diVerent treatments (Zar 1999). The tests donot assume that each site and date is equal, only that thesampling eVort within a site-date event is equal. Here, theassumption is that the uniform nature of the reefs, soundsystems, moorings and sites, and the alternation of treat-ments between experimental patch reefs validate thisapproach.

Results

Experiment 1: Reef noise vs. silent

Over six nights and at four sites during the November newmoon, a total of 22 replicates (six at A and B, Wve at C andD) were obtained. In total, 79 adults (9 species from 4 fam-ilies) and 166 juveniles (21 species from 13 families) werecollected (Table 1). Of these, 53% of the adults and 72% ofthe juveniles were collected from reefs with broadcastsound. There was no obvious trend in the arrival of adultWsh with respect to treatment, whereas signiWcantly morejuveniles from three taxa (Apogonidae, �2 P < 0.01; Gobii-dae and Pinguipedidae, �2 P < 0.05) were collected at thenoisy reefs. Analysis of the juveniles using Wilcoxon’spaired tests identiWed a increase in diversity, both by num-ber of families and number of species, on the noisy reefs ona per site-night basis (Wilcoxon’s P < 0.01), as well as con-Wrmation that the apogonids, gobiids and pinguipedids pref-erentially selected the noisy reefs (Wilcoxon’s P < 0.05).

Fig. 3 Frequency-intensity analyses of the three sound treat-ments used in this study. The full spectrum recording was used in Experiment 1, and the high and low frequency recordings (80% of broadcast noise > 570 Hz, 80% < 570 Hz respectively) used in Experiment 2. Actual broadcast sound levels were maintained at 156 dB re 1 �Pa at 1 m in all three treatments

0

0.5

1

1.5

2

2.5

0 500 1000 1500 2000 2500 3000 3500

Frequency (Hz)

Inte

nsity

(m

V)

Full Spectra

LowFrequency

HighFrequency

570 Hz

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There were no families represented in either life stage thatsigniWcantly preferred the silent reefs.

Experiment 2: High frequency vs. low frequency reef noise vs. silent

The three-way experiment ran for eight nights during theDecember new moon. Although one replicate at site A waslost due to the moorings dragging on the spring tide, andanother at site A due to equipment Xooding, a total of 13replicates (Wve at A and eight at D) were obtained. In total,122 adults (11 species from 6 families) and 372 juveniles(41 species from 18 families) were collected (Table 2). Ofthe adults, 30% arrived on the high frequency reefs, 52% onlow frequency reefs and 19% on silent reefs. When analy-sed on a pairwise site-date level, Friedman’s tests identiWedconsistent diVerences in the overall diversity of adults asso-ciated with each treatment at the species level (P < 0.05).There were signiWcant diVerences (P < 0.01) in overall

numbers between treatments in the adult Gobiidae andBlenniidae. The trend was for a greater number of adultgobiids on low frequency reefs than silent ones (37:15), anda greater number of adult blenniids on low frequency reefscompared to both high frequency and silent reefs (16:5:5).

An overall preference for the low frequency reefs wasalso seen in the juvenile Wsh, with 30% associated withhigh frequency reefs, 46% with low frequency reefs, and24% with silent reefs (Table 2). The juveniles of severalfamilies showed signiWcant preferences for certain treat-ments. Apogonids preferred noisy reefs (�2 P < 0.01), with71% arriving at low frequency and 19% at higher frequency

Table 1 Summary of collections of adult and juvenile coral reef Wshesfrom patch reefs constructed oV Lizard Island, Great Barrier Reef,broadcasting reef noise or with silent “dummy” rigs

Results of Chi-squared tests on total numbers and Wilcoxon’s pairedtests on site-date replicates (n = 22) are shown (see “Materials andmethods” for details), with ** indicating P < 0.01, * indicatingP < 0.05, and – indicating P > 0.05

Low catches prevented analysis of some rarer families (indicated by #)

Sound Silent Total �2 Wilcoxon’s

Adults

Total no. of families 4 4 4 –

Total no. of species 6 9 9 –

Gobiidae 23 20 43 – –

Blenniidae 14 9 23 – –

Pomacentridae 4 7 11 – –

Apogonidae 1 1 2 – –

Juveniles

Total no. of families 13 9 13 **

Total no. of species 19 14 21 **

Apogonidae 59 20 79 ** *

Gobiiedae 26 12 38 * *

Mullidae 12 6 18 – –

Pinguipedidae 7 1 8 * *

Acanthuridae 3 2 5 – –

Blenniidae 3 2 5 – –

Synodontidae 2 1 3 – –

Lutjanidae 2 0 2 # –

Pomacentridae 1 1 2 – –

Serannidae 1 1 2 – –

Tetraodontidae 2 0 2 # #

Balistidae 1 0 1 # #

Labridae 1 0 1 # #

Table 2 Summary of collections of adult and juvenile coral reef Wshesfrom patch reefs broadcasting high frequency or low frequency reefnoise or with silent “dummy” rigs

Results of Chi-squared tests on total numbers and Freidman’s pairedtests on site-date replicates (n = 13) are shown (see “Materials andmethods” for details), with ** indicating P < 0.01, * indicatingP < 0.05, and – indicating P > 0.05

Low catches prevented analysis of some rarer families (indicated by #)

High Low Silent Total �2 Freidman’s

Adults

No. of families 4 5 5 6 –

No. of species 8 10 9 11 *

Gobiidae 26 37 15 78 ** –

Blenniidae 5 16 5 26 ** –

Unknown 4 8 1 13 – –

Labridae 1 1 1 3 – –

Apogonidae 0 1 0 1 # #

Pomacentridae 0 0 1 1 # #

Juveniles

No. of families 13 14 16 18 –

No. of species 25 28 24 41 –

Apogonidae 23 86 12 121 ** –

Gobiidae 30 26 12 68 * –

Blenniidae 14 22 16 52 – –

Monacanthidae 11 7 10 28 – –

Synodontidae 7 7 8 22 – –

Pomacentridae 4 6 10 20 – –

Unknown 7 6 6 19 – –

Acanthuridae 9 3 1 13 * –

Lethrinidae 2 4 1 7 – –

Serranidae 1 1 3 5 – –

Pinguipedidae 0 1 3 4 – –

Siganidae 2 1 1 4 – –

Tetraodontidae 0 1 2 3 – –

Balistidae 1 1 0 2 – –

Carangidae 0 0 1 1 # #

Labridae 0 0 1 1 # #

Platycephalidae 1 0 0 1 # #

Scorpaenidae 0 0 1 1 # #

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reefs compared to 10% at silent reefs. Gobiids also showeda non-random distribution between treatments (�2 P < 0.05),with the high frequency reefs favoured over the silent reefs.Acanthurids preferred high frequency reefs (�2 P < 0.05)compared to the other two treatments. In parallel withExperiment 1, there were no families represented in eitherlife stage that signiWcantly preferred the silent reefs.

Discussion

This study demonstrates that the behaviour of juvenile andadult coral reef Wshes is sometimes inXuenced by the acous-tic environment (or “soundscape”). It also shows that theseWshes can determine the direction of a sound, and movetowards its source. Finally, it clearly suggests that the juve-nile stages of at least three families of reef Wshes (Apogoni-dae, Gobiidae and Pinguipedidae) use the natural sounds ofreefs to locate and migrate to new habitat. It is possible thatfurther sampling to increase sample sizes may have turnedsome of the trends, which were seen in other families intostatistically signiWcant responses. However, there is a trade-oV between building replicates to detect signiWcantresponses in the rarer taxa and the number of more commonWsh that must be sacriWced in order to achieve this. It ishoped that the sampling eVort in this study represents anappropriate balance between these conXicting issues.

At night, vision has limited potential for orientation,whereas sound levels are at their greatest, so the sound-scape around reefs is at its most clearly deWned (McCauleyand Cato 2000). Acoustic information available to Wsheswill include both qualitative and quantitative elements. Thequality of the noise will depend upon the position of thereef with respect to prevailing weather conditions (e.g.,wave action) and the inhabitants on the reef producing thebiological noise. Animals from four phyla produce biologi-cal noise. Among the molluscs, mussels have been found toproduce sounds by stretching and breaking the byssalthreads attaching them to rocks, creating “mussel crackle”in the range of 1–4 kHz (Fish and Mowbray 1970). A “fry-ing noise” originating from echinoderms (50–5k Hz, peakat 2 kHz), including the tropical urchin Diadema antilla-rum, has been reported (e.g. Tolimieri et al. 2000). Thisnoise is probably produced in the calcareous Aristotle’slantern during feeding. Predominantly urchin-generatednoise was used to attract settlement-stage tripterygiids tolight traps in New Zealand (Tolimieri et al. 2000). A largeproportion of the higher frequency noise is produced by thearthropods, in particular the snapping shrimps (Versluiset al. 2000). This noise is normally a low-level higher fre-quency (2.5–200+ kHz) background crackle (see Fig. 1 inSimpson et al. 2004). The fourth phylum to contribute tobiological noise in the sea is the chordates (predominantly

Wsh on reefs, but also occasionally pinnepeds and ceta-ceans). Many reef Wsh produce noises at low frequencies(Sciaenidae drumming: 200–400 Hz; unknown banging:280–420 Hz; Holocentridae popping: 400–700 Hz), andholocentrids are known to communicate while hunting atnight using “popping” noises produced in excess of 156 dBre 1 �Pa at 1 m (McCauley and Cato 2000). Daytime-activepomacentrids have also been shown to communicate usingsound (350–1,000 Hz), for both courtship and territorialadvantage (Myrberg et al. 1986, 1993; Kenyon 1994; Mannand Lobel 1997, 1998; Myrberg 1997). Many reef Wshes areknown to produce noises, their abilities often reXected intheir common names: e.g., drums, grunts and croakers. Itmust be the case, although it is yet unproven, that reefs willhave diVerent acoustic signatures according to the commu-nities they support.

The quantity of noise at a given location in the sound-scape will depend upon the level of sound being produced,and the distance to these sources. Importantly, the distanceto the source also aVects the comparative magnitudes of theparticle motion component of sound (limited to the near-Weld), and the radial particle velocity and pressure compo-nents (which extend into the far-Weld). In this study it wasnot possible to disentangle the relative importance of eachof these processes (see Montgomery et al. 2006 for areview). Compared to other cues (e.g., chemicals), soundattenuates in water in a more predictable manner, irrespec-tive of current. As such, this gradient may provide a valu-able guide both for oVshore movement of settlement-stagelarvae during the day (Leis et al. 1996), and onshore move-ment towards the source at night (Stobutzki and Bellwood1998; Tolimieri et al. 2000, 2004; Leis et al. 2003; Simpsonet al. 2004, 2005; Leis and Lockett 2005). Factoring in thenoise from abiotic sources (e.g., wave action), it is clearthat the soundscape will be highly heterogeneous, poten-tially providing valuable information to coral reef Wshes forrelocation or nocturnal orientation.

This study set out to investigate whether the juvenile andadult stages of coral reef Wshes use the sounds of reefs toidentify and move towards settlement sites. In parallel withSimpson et al. (2005), the potentially confounding factor ofthe innate or adaptive attraction to light was avoided (incontrast to Tolimieri et al. 2000; Leis et al. 2003; Simpsonet al. 2004), and instead the orientation behaviour to patchreefs solely in response to sound cues was isolated. SuchartiWcially constructed “patch reefs” have been used previ-ously to study both rates of natural recruitment (Milicichet al. 1992; Meekan et al. 1993), and the importance ofchemical cues for settling Wshes (Sweatman 1988).

No speciWc response in the adult Wshes to the full spec-trum noisy reefs over the silent reefs was found. However,the collections of adult Wshes in the second experimentwere slightly larger, with an average of 0.8 individuals per

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reef (compared to 0.6 individuals per reef in Experiment 1).In this second experiment, an increased diversity of adultWshes at the species level was found on the low frequencyreefs. In addition, adults from two taxa (Gobiidae and Blen-niidae) responded towards the low frequency reefs. The lowfrequency component of reef noise is predominated by Wsh-generated noise, so these results perhaps suggest a responseof these families to the pre-recorded Wsh community. Thecombined results of these two experiments may indicatethat adult gobiids and blenniids will only respond to noisewhen the high frequency element is less prominent; how-ever, this hypothesis would require testing using an avoid-ance experiment.

Positive responses by a number of juvenile Wshes to reefsbroadcasting full spectrum reef noise over silent reefs wereidentiWed. Overall numbers were signiWcantly greater onreefs with noise in the apogonids, gobiids and pinguipedids,and on a per-replicate basis there was also an increase indiversity at the species level. Experiment 2 identiWed a pos-itive response in the juvenile apogonids toward the reefsbroadcasting low frequency sounds. The preferential move-ment of juveniles towards reefs broadcasting low frequencynoises was also seen in the diversity of collections at thespecies level. In contrast, gobiids preferred noisy reefs, butwere less selective with respect to the noise frequency,while the rarer acanthurids preferred the reefs broadcastinghigh frequency noises.

In parallel with previous studies on settlement-stage reefWshes (Leis et al. 2003; Simpson et al. 2004, 2005), theseresults suggest that the heterogeneity of the soundscapemay be important to Wshes from later life stages movingamong benthic habitats (e.g., reef, sand Xat, mangrove andseagrass; Nagelkerken et al. 2000). Neighbouring habitatsare likely to sound diVerent, since the noises producedresult from the suite of animals in residence, so the sound-scape may be of value in selecting an appropriate commu-nity and habitat for each life stage (settlement site, nurserygrounds, juvenile feeding grounds, conspeciWc colonies,and available territories). For example, sound may beimportant to the Hawaiian damselWsh Dascyllus albisellawhich is highly vocal during social interactions (Mann andLobel 1998), since it recruits Wrst to a juvenile group, thenmoves on to an adult population on reaching adulthood(Booth 1995). This study also identiWed a diversity ofresponses by diVerent Wshes to components of the sound-scape. This behaviour may be driven by diVerent habitat- orcommunity-speciWc selection criteria for the behaviour, butmay also be due to the physiology and neuroanatomy of thehearing apparatus. Meta-studies of Wsh hearing researchdemonstrate the considerable variation in thresholds andspectral ranges of hearing between families (Fay and Sim-mons 1998). Elucidating the extent to which sensory limita-tion compared to adaptive response controls this behaviour

will greatly improve our understanding of the movement ofjuvenile and adult Wshes with respect to their soundscapes.

There are potential management issues raised by thisstudy. First, that post-settled reef Wshes can be attracted toartiWcial reefs using noise may one day provide a valuablemanagement tool for Wsheries and conservation managers(a “Pied Piper” approach). Second, it shows that bothchronic and acute anthropogenic noise pollution couldinXuence natural behaviour. Examples of chronic noise pol-lution around reefs include the noise from supertankers(205 dB re 1 �Pa at 1 m), ship engines, hulls and propellers(160–170 dB re 1 �Pa at 1 m), small boat traYc (152–162 dB re 1 �Pa at 1 m), and mining and drilling operations(Richardson et al. 1995). Exposure to white noise at 170 dBre 1 �Pa causes temporary threshold shifts in goldWsh(Carassius auratus) of 13–20 dB (Smith et al. 2006), whicheVectively reduces the detectable distance of a sound by upto 85% (6 dB loss for doubling of distance). There is evi-dence that acute sound sources can also aVect hearing inWshes. Pink snapper (Pagrus auratus) exposed to air-gunblasts (used in marine seismic petroleum exploration,226 dB re 1 �Pa at 1 m) sustained extensive damage to thehair cells in the sensory epithelia surrounding the otoliths,which showed no signs of repair even after 58 days(McCauley et al. 2003). Estimates indicate that anthropo-genic input increased the levels of ambient noise in theworld’s oceans by as much as 10 dB, or one full order ofmagnitude, between 1950 and 1975 (Jasny 1999). Thistrend is likely to have continued with the increase in ship-ping and mining over the past 30 years. A third potentialissue, that will be challenging to measure or quantify, is theimpact of Wshing or pollution that targets or aVects compo-nents of the reef community responsible for producing thenatural sounds that Wsh are using as cues. This may havesecondary but fundamental eVects on the sorting of reefWshes and hence the structure of communities. These issuesmust be the focus of future studies in order to conserve thecues that Wshes naturally use to guide their movements.

Acknowledgments We thank the staV at the Lizard Island ResearchStation, M. Wolter, C. Simpson, and N. Larsen for assistance in theWeld, C. Radford for analysis of sound treatments, and A. Heenan,C. Johansson, and four anonymous reviewers for valuable comments onthe manuscript. This work was supported by a Natural EnvironmentResearch Council postdoctoral fellowship, the Fisheries Society of theBritish Isles and the British Ecological Society (to S.D.S.), the Mars-den Fund (to A.J. and J.C.M), and the Australian Institute of MarineScience (to M.G.M.).

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