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The influence of various reef sounds on coral-fish larvae behaviour

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Abstract

The swimming behaviour of coral-reef fish larvae from 20 species of 10 different families was tested under natural and artificial sound conditions. Underwater sounds from reef habitats (barrier reef, fringing reef and mangrove) as well as a white noise were broadcasted in a choice chamber experiment. Sixteen of the 20 species tested significantly reacted to at least one of the habitat playback conditions, and a range of responses was observed: fishes were (1) attracted by a single sound but repelled by none (e.g. white-banded triggerfish Rhinecanthus aculeatus was attracted by the barrier-reef sound), (2) repelled by one or more sounds but attracted by none (e.g. bridled cardinalfish Pristiapogon fraenatus was repelled by the mangrove and the bay sounds), (3) attracted by all sounds (e.g. striated surgeonfish Ctenochaetus striatus), (4) attracted and repelled by several sounds (e.g. whitetail dascyllus Dascyllus aruanus was attracted by the barrier-reef sound and repelled by the mangrove sound) and (5) not influenced by any sound (e.g. convict surgeonfish Acanthurus triostegus). Overall, these results highlight two settlement strategies: a direct selection of habitats using sound (45% of the species), or a by-default selection by avoidance of certain sound habitats (35%). These results also clearly demonstrated the need to analyse the influence of sounds at the species-specific level since congeneric and confamilial species can express different behaviours when exposed to the same sounds. © 2015 The Fisheries Society of the British Isles.
Journal of Fish Biology (2015)
doi:10.1111/jfb.12651, available online at wileyonlinelibrary.com
The inuence of various reef sounds on coral-sh larvae
behaviour
E. Parmentier*, L. Berten*, P. Rigo*, F. Aubrun, S. Nedelec§, S.
D. Simpson§and D. Lecchini
*Laboratoire de Morphologie Fonctionnelle et Evolutive, AFFISH-RC, Institut de chimie, Bât.
B6c, Université de Liège, B-4000 Liège, Belgium, USR 3278 CNRS-EPHE, CRIOBE, 97829
Moorea, French Polynesia, §School of Biological Sciences & Cabot Institute, University of
Bristol, Woodland Road, Bristol, BS8 1UG, U.K., Biosciences, College of Life &
Environmental Sciences, University of Exeter, EX4 4QD, U.K. and Laboratoire d’Excellence
"CORAIL", 97829 Moorea, French Polynesia
(Received 7 October 2014, Accepted 28 January 2015)
The swimming behaviour of coral-reef sh larvae from 20 species of 10 different families was tested
under natural and articial sound conditions. Underwater sounds from reef habitats (barrier reef, fring-
ing reef and mangrove) as well as a white noise were broadcasted in a choice chamber experiment.
Sixteen of the 20 species tested signicantly reacted to at least one of the habitat playback conditions,
and a range of responses was observed: shes were (1) attracted by a single sound but repelled by
none (e.g. white-banded triggersh Rhinecanthus aculeatus was attracted by the barrier-reef sound),
(2) repelled by one or more sounds but attracted by none (e.g. bridled cardinalsh Pristiapogon frae-
natus was repelled by the mangrove and the bay sounds), (3) attracted by all sounds (e.g.striated
surgeonsh Ctenochaetus striatus), (4) attracted and repelled by several sounds (e.g.whitetaildascyl-
lus Dascyllus aruanus was attracted by the barrier-reef sound and repelled by the mangrove sound) and
(5) not inuenced by any sound (e.g.convictsurgeonshAcanthurus triostegus). Overall, these results
highlight two settlement strategies: a direct selection of habitats using sound (45% of the species), or
aby-defaultselectionbyavoidanceofcertainsoundhabitats(35%).Theseresultsalsoclearlydemon-
strated the need to analyse the inuence of sounds at the species-specic level since congeneric and
confamilial species can express different behaviours when exposed to the same sounds.
© 2015 The Fisheries Society of the British Isles
Key words: acoustic cues; coral reef; habitat; orientation; settlement; teleosts.
INTRODUCTION
Coral-reef shes have a complex life cycle, characterized by a pelagic larval stage,
followed by benthic juvenile and adult stages (Leis & McCormick, 2002). Reef col-
onization takes place mainly during the night and corresponds to the passage of the
larvae from the ocean to a reef (Dufour & Galzin, 1993), quickly followed by the set-
tlement in an adequate habitat (Lecchini, 2005). These steps are generally related to
morphological and physiological modications to adapt to important environmental
changes related to the transition from pelagic life in open sea to benthic life on the reef
Author to whom correspondence should be addressed. Tel.: +3243665024; email: E.Parmentier@ulg.ac.be
1
©2015TheFisheriesSocietyoftheBritishIsles
2E. PARMENTIER ET AL.
(McCormick et al., 2002; Parmentier et al., 2004). During the rst few hours following
the colonization and settlement, the mortality rate is high, with up to 60% mortality
on the rst day post-colonization (Doherty et al.,2004),implyingthattheabilityto
quickly nd and settle in an appropriate habitat is highly important for larval survival
(Kaufman et al.,1992;Lecchini,2005).
The settlement habitat is known to be chosen according to various characteristics,
such as conspecic presence, quality of habitat or absence of predators (Öhman et al.,
1998; Lecchini et al., 2007a;Ben-Tzviet al., 2009). Orientation towards suitable habi-
tats appears possible with the use of chemical (Atema et al.,2002;Lecchiniet al.,2005;
Arvedlund & Takemura, 2006; Dixson et al.,2008),visual(Leis&Carson-Ewart,
2003; Lecchini et al.,2007b; Igulu et al.,2011)andacousticcues(Tolimieriet al.,
2000; Leis et al.,2003;Simpsonet al.,2004;Holleset al.,2013).
The inuence of reef sound on settling shes has become a subject of particular inter-
est in the past few years, since Stobutzki & Bellwood (1998) showed that sh larvae
could use sound as a cue for orientation. Several experiments using choice chambers
have been used in recent years and highlighted an attractive effect of broadcasted reef
noise (Tolimieri et al.,2004)andtheinuenceofarticialtonenoiseonshbehaviour
(Simpson et al.,2010;Holleset al.,2013).Theuseofsoundtolocatehabitathasalso
been recently shown at Lizard Island (Australia) where juveniles are signicantly more
attracted to patch reefs with lagoon or fringing-reef sound broadcast than to patch reefs
with no playback sound (Radford et al.,2011).
In all these studies, differences were observed at the family level. For example, Poma-
centridae were preferentially found on patch reefs broadcasting fringing-reef sound
than on other treatments (Radford et al.,2011).Thestudyofresponsesatthefamily
level, however, is potentially oversimplied. The number of species studied in the same
taxa can considerably modify the results when they are all pooled to consider the fam-
ily level. In the above studies, Pomacentridae were, overall, signicantly attracted by
aparticularsoundplayback,butitdoesnotimplythatallPomacentridaespeciesshow
the same kind of behaviour because species have different ecological niches, meaning
that they may not be sensitive in the same way to different cues. This remark is par-
ticularly important as the sounds emitted from different locations (fringing reef, back
reef and lagoon) have revealed differences in the temporal and frequency composition
and in sound levels (Radford et al., 2014). At this stage, species-specic reactions to
different kinds of reef sounds are not known. In this study, the inuence of broadcasted
natural sounds (fringing-reef, barrier-reef and mangrove sounds) and articial white
noise on the sh behaviour during their settlement stage was tested. In particular, the
ability of 21 sh species from 10 families to use the sounds of three specic habitats as
acuefortheselectionoftheirsettlementhabitatisdetermined.Moreover,itisshown
that the study at the family level can mask behaviour at the species-specic level.
MATERIALS AND METHODS
This study was conducted at Moorea (French Polynesia; 1731S; 14951W) from Febru-
ary to April 2011 and 2012 using sh larvae captured in crest nets (Lecchini et al.,2006).A
total of 1449 sh larvae belonging to 21 species and 10 families were tested (see Table I), with
a sample size of six to 25 shes per species for each sound treatment. Due to a lack of lar-
vae, one test (the white-noise test) was not conducted on whitetail dascyllus Dascyllus aruanus
(L. 1758) and Bennet’s sharpnose buffer Canthigaster bennetti (Bleeker 1854). The total lengths
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Biol ogy 2015, doi:10.1111/jfb.12651
REEF-SOUND INFLUENCE ON FISH LARVAE BEHAVIOUR 3
Table I. Experimental results from choice-chamber tests on several species of coral-reef sh larvae, showing habitats signicantly selected by each
sh species (𝜒2homogeneity test and P-value), with putative strategy and comparison with eld observations (Lecchini, 2005; Lecchini & Galzin, 2005)
Experimental results Theory Field observations
Attracted by (P-value) Deterred by (P-value) Selected habitat Strategy Settlement habitat
Acanthuridae Acanthurus triostegus None None X X FR
Ctenochaetus striatus All None All A BR, FR
Apogon doryssa ––
Apogon sp. BR (<005) None BR A BR, FR
Apogonidae Ostorhinchus angustatus B(<005) None B A BR, FR
Pristiapogon exostigma None MG (<0001) BR, FR B BR, FR
Pristiapogon fraenatus None MG (0033), B (<005) BR, FR B BR
Balistidae Rhinecanthus aculeatus BR (<005) None BR A BR, FR
Chaetodontidae Chaetodon citrinellus MG (<005) BR (<005) MG ABR
Gobiidae Valenciennea strigata None None X X BR
Myripristis kuntee FR (<001) None FR A FR
Holocentridae Neoniphon argenteus None BR (<005), MG (<0001) FR B FR
Sargocentron microstoma BR (<005) None BR A BR
Sargocentron spiniferum B(<005) None B A BR
Microdesmidae Ptereleotris microlepsis None BR (<005) FR, MG B BR, FR
Abudefduf sexfasciatus None FR (0028), MG (0028) BR B BR, FR
Pomacentridae Chromis viridis None None X X FR
Chrysiptera leucopoma None B (<001) BR, FR, MG B BR
Dascyllus aruanus BR (<005) MG (<001) BR A BR, FR
Scorpaenidae Scorpaenodes guamensis None None X X BR, FR
Tetraodontidae Canthigaster bennetti None FR (<005), B (<005) BR, MG B BR
, no reaction to tested sounds; , total or partial correspondence between eld observations and predicted habitat choice; , eld observations and predicted habitat
choice do not correspond; B, bay; BR, barrier reef; FR, fringing reef; MG, mangrove; strategy A, direct selection of sound habitat; strategy B, by-default selection of
remaining sound habitat; X, no strategy given due to no reaction to tested sounds. Habitat sounds were not tested on A. doryssa due to environmental bias highlighted by
the side bias experiment. White noise was not tested on D. aruanus and C. bennetti due to the lack of larvae.
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Bio logy 2015, doi:10.1111/jfb.12651
4E. PARMENTIER ET AL.
(LT) of the tested shes varied with species, ranging from c.05cmfor thesmallest, e.g. blue
green damselsh Chromis viridis (Cuvier 1830) and D.aruanus,toc.7cmforsmallmouth
squirrelsh Sargocentron microstoma (Günther 1859).
SOUND TREATMENTS
Playback sounds of fringing reef, barrier reef and mangrove were recorded at dusk between
February and April 2010 on the north coast of Moorea. Sounds were recorded with a calibrated
broadband hydrophone (High Tech HTI-96-MIN, with in-built preamplier, sensitivity 164 dB
re 1 V μPa1, frequency range 2 Hz to 30kHz. High Tech Inc.; www.hightechincusa.com), con-
nected to a solid-state calibrated recorder (Edirol R-09HR, 24 bit, sample rate 441kHz.Roland
System Group; www.rolandsystemsgroup.com). For each habitat, ve GPS locations were cho-
sen. Locations within each habitat were separated by 10100 m, and present similar charac-
teristics (i.e. depth, coral structures and biotic community). Recordings of 1 min duration were
taken at each point, with replications on three different days. A control sound was recorded at
5 m depth in the middle of Opunohu Bay, a natural biotope of low interest for reef-sh larvae
(Lecchini & Galzin, 2005). In order to avoid the sound of waves slapping on a boat or other
boat-related noise, recordings were taken from a plastic kayak. Sound les were cleaned of any
unnatural sound (e.g. boats passing away, paddle sounds and cable rubbing) using the Avisoft
SASLab Pro (Avisoft Bioacoustics; www.avisoft.com). Small sections (3 s duration) of each
le were randomly rearranged to create a typical 5 min duration sample of each habitat sound
(Fig. 1). The bay sound was a natural sound similar to white noise up to 1000 Hz, with a slight
increase at higher frequencies. Fringing-reef and barrier-reef sound express similar spectrogram
patterns to one another, although intensity around 300Hz is 10 dB higher for barrier reef than
for fringing reef, while it is lower for frequencies around 1200 Hz. As mangrove sound is mainly
silent but with sparse clicks of high frequency (10 kHz and higher), and to avoid any background
noise effect of the experimental site, silences were removed to increase the rate of clicks on the
soundtrack. Thus, this sound could not completely correspond to the natural sound from the
mangrove. Due to the use of a loudspeaker at 10m from the choice chamber, a high pass lter of
100 Hz was applied on all playback sound to avoid near-eld effects (Mann, 2006). An articial
white noise (100 Hz22 kHz) was created with Avisoft SasLab Pro.
EXPERIMENTAL DESIGN
Fish larvae collected from the crest nets (Lecchini et al., 2004) at sunrise were transferred to
a laboratory aquarium (59 cm ×39 cm, water depth: 14 cm, CRIOBE station) that was placed
on sound insulating material (5 mm thick polystyrene), away from passing researchers and with
a constant supply of oxygenated seawater piped in below the surface to keep aquarium noise
to a minimum [background noise =783 peak sound pressure spectrum level (SPL) in dB re 1
μPa2Hz1between 200 and 3000 Hz from a 30 s sample, fast Fourier transform (FFT) length
1024, geometric mean across all frequency bands between 200 and 3000 Hz=649dBre1μPa2
Hz1](Holleset al., 2013). As most larval coral-reef shes colonize at night (Lecchini et al.,
2004; Simpson et al., 2005, 2008), shes were used in choice-chamber experiments (Fig. 2) in
the lagoon adjacent to the CRIOBE research station (http://usr3278.univ-perp.fr/moorea/) the
following night.
Experiments took place on a quiet and sandy lagoon on the north coast of Moorea. Larvae
were tested in a choice chamber experiment (Simpson et al., 2010; Holles et al.,2013)made
of three parallel cylindrical plastic polythene tubes (360 cm length ×30 cm diameter), sepa-
rated from each other by 060 m. In the middle of the chamber, a sealable opening allowed
introduction of larvae to the centre of each chamber, while the chamber ends were closed by
1 mm mesh (Fig. 2). The experimental chambers were suspended beneath the water surface,
parallel to the shore and the barrier reef to control for potential natural directional cues. The
experiments were conducted in a water depth that varied between 12and15m withthe tide.
Underwater loudspeakers (Lubell UW30, frequency response from 01Hz to 10kHz. Univer-
sity Sound; www.lubell.com) were placed at 10m from both ends of the experimental chambers
extremities. Speakers were connected to audio ampliers (Formula F-102), powered by a 12V
216 Ah battery, and linked to a music player (MpMan Mpub330; www.mpmaneurope.com),
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Biol ogy 2015, doi:10.1111/jfb.12651
REEF-SOUND INFLUENCE ON FISH LARVAE BEHAVIOUR 5
110 (a) (b)
(c)
(e)
(d)
100
90
80
70
100 1000
Hz
100 1000
Hz
110
100
90
80
70
dB re 1 µPa2 Hz–1
110
100
90
80
70
Fig. 1. Power spectrum of tested sounds (a) barrier reef, (b) fringing reef, (c) mangrove, (d) white noise and (e)
bay, played in the experimental choice chamber device [hamming window, fast Fourier transform (FFT)
size 512, applied on a 5 s selection].
containing the sound les in WAV format. The whole electronic device was in a oating water-
proof box, moored on the sandy bottom. The intensity of playback was at least 90 dB re 1μPa
RMS (root mean square) to ensure that it was above the local ambient noise oor (recorded at
maximum 80 dB re 1μPa RMS).
One larva at a time was used per chamber, and each sh was used only once. Six dual sound
treatments were applied (Table II). As the control sound (bay sound) was used for every treat-
ment, and to avoid as much as possible any environmental bias, the side of the chamber where
the control sound was played was balanced from test to test. The order of treatments was ran-
domized each night, as well as sh species position in the three chambers (nearest to the shore,
in the middle and farthest from the shore).
After sh larvae were placed in the chambers, a settling period of 2min silence was observed
before 3 min of playback sound. At the end of each trial, the experimental chambers were divided
and closed into three sections of equal length, after which the position of the larva in the cham-
ber was established by snorkellers using underwater torches. The location of the shes in the
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Bio logy 2015, doi:10.1111/jfb.12651
6E. PARMENTIER ET AL.
10 m
Opening
Mesh
Sound speaker
Proof box with music
player and amplier
Choice chambers
360 cm
Fig. 2. Experimental choice chamber used to test the attractiveness and repelling effect of playback sounds on
coral-reef larvae. Choice chamber was made of three parallel cylindrical plastic tubes (30cm diameter),
separated from each other by 060 m. They were suspended in a water depth between 12and15 m. Under-
water loudspeakers were placed at 10 m from both ends of the experimental chamber extremities. Music
player and amplier were placed in a oating waterproof box, moored on the bottom.
chamber was recorded as near, middle and far from the speaker playing the sound of interest
(i.e. the sound played against the control sound). After being tested, the larvae were released
into the lagoon.
STATISTICAL ANALYSIS
Fish distributions in the chambers at the end of the experiments were analysed using 𝜒2tests.
The control for side bias (bay sound v. bay sound) assessed whether larvae had a directional bias
when same sound was played on both sides. If shes were statistically more present on one side
than the other, it was assumed the experimental environment had a bias effect on larvae due to
other cues than sound (e.g. wave, celestial or magnetic cues) and the species was discarded from
the experiment. For the 21 species tested, this situation occurred only for longspine cardinalsh
Apogon doryssa (Jordan & Seale 1906). The control sound test (bay sound v. no playback)
aimed to test the inuence of bay sound on larvae behaviour. The inuence of bay sound, if
any, was considered for subsequent analysis of white noise and habitat sounds. The white-noise
test (bay sound v.whitenoise),BRtest(baysoundv. barrier-reef sound), FR test (bay sound v.
fringing-reef sound) and MG test (bay sound v. mangrove sound) aimed to test the inuence of
an articial noise and natural habitat sounds on reef sh larvae behaviour.
The analysis of the species distribution in the chamber was conducted according to the distri-
bution observed in the side-bias test. Firstly, for species evenly distributed in all three compart-
ments of the chamber during the side-bias test, the compartment in which the sh was found at
the end of the white-noise test or habitat-sound test was recorded (far from or near to the speaker
broadcasting the tested sound, or in the middle). To test the attractiveness of habitat sound in
this compartment, the number of shes in it was compared (𝜒2homogeneity test) to a theoret-
ical distribution of 033:066 (the sum of shes in the unselected compartments). Secondly, for
Table II. The six experimental sound treatments applied to several species of coral-reef sh
larvae in the choice chambers
Test Dual sound treatment Purpose
Side bias Bay sound v. bay sound To test environmental bias
Control sound Bay sound v. no playback To test inuence of the control sound
White noise Bay sound v. white noise To test the inuence of articial noise
FR Bay sound v. fringing-reef sound To test the inuence of habitat sounds
BR Bay sound v. barrier-reef sound To test the inuence of habitat sounds
MG Bay sound v. mangrove sound To test the inuence of habitat sounds
FR, fringing reef; BR, barrier reef; MG, mangrove.
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Biol ogy 2015, doi:10.1111/jfb.12651
REEF-SOUND INFLUENCE ON FISH LARVAE BEHAVIOUR 7
species with a half and half distribution in the extremities during the side-bias test, the shes
found in the centre compartment at the end of the sound test were not taken in account, and the
distribution of shes in extremities was compared (𝜒2homogeneity test) to a 05:05 theoretical
distribution.
A sound was said to have an attractive or deterrent effect on sh behaviour if the species did
not show a preference for one side or the other during the control-sound test, but was found
signicantly more often in the compartment nearest to the loudspeaker broadcasting the test
sound (attractive effect) or in the farthest compartment (deterrent effect). If the species showed
a preference for the compartment near the bay loudspeaker during the control-sound test, the
attractive effect of tested sound was dened the same way, but the deterrent effect would not be
differentiated from an inherent attractiveness of bay sound. Also, if the species was found signif-
icantly more often in the compartment near the silent loudspeaker during the control-sound test,
an attractive effect of the tested sound would notbe differentiated from an inherent repulsiveness
of bay sound.
RESULTS
SIDE-BIAS TEST (BAY SOUND V.BAYSOUND)
When the same sound was played at both ends of the choice chambers, 16 species
showed an even distribution (033:033:033), suggesting that they did not have prefer-
ence for a specic compartment. This was not the case, however, for convict surgeon-
sh Acanthurus triostegus (L. 1758), A.doryssa,C.viridis,white-bandedtriggersh
Rhinecanthus aculeatus (L. 1758) and S.microstoma (𝜒2homogeneity test, d.f. =2,
P<005). The larvae of these species (except A.doryssa)weredistributedequally
between both extremities (05:0:05) (𝜒2homogeneity test, d.f. =1, P<005). Because
A.doryssa did not display a symmetrical distribution, this species may have poten-
tially been affected by an environmental bias. Consequently, it was discarded in further
experiments.
CONTROL-SOUND TEST (BAY SOUND V.NOPLAYBACK)
Six species statistically reacted (𝜒2homogeneity test, d.f. =1, P<005) under
the inuence of bay sound, tested against no playback (meaning natural sound
background). Striated surgeonsh Ctenochaetus striatus (Quoy & Gaimard 1825),
broadstriped cardinalsh Ostorhinchus angustatus (Smith & Radcliffe 1911) and sabre
squirrelish Sargocentron spiniferum (Forsskål 1775) were attracted by bay sound,
while bridled cardinalsh Pristiapogon fraenatus (Valenciennes 1832), surge dam-
selsh Chrysiptera brownriggii (Bennett 1828) and C.bennetti were repelled by it. The
remaining 14 species were neither signicantly attracted nor deterred by the bay sound.
WHITE-NOISE TEST (BAY SOUND V. WHITE NOISE)
Four of the 18 species tested showed a signicant response to white-noise (𝜒2
homogeneity test, d.f. =1, P<005). Ctenochaetus striatus,speckledbutterysh
Chaetodon citrinellus Cuvier 1831 and Guam scorpionsh Scorpaenodes guamensis
(Quoy & Gaimard 1824) were more likely to be found in the section of the chamber
closest to the loudspeaker playing white noise, while O.angustatus was found more
frequently on the bay sound side, conrming the attractive effect of bay previously
highlighted by the control-sound test.
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Bio logy 2015, doi:10.1111/jfb.12651
8E. PARMENTIER ET AL.
HABITAT-SOUND TEST (BAY SOUND V. HABITAT SOUND)
The fringing-reef sound signicantly attracted C.striatus and shoulderbar soldiersh
Myripristis kuntee Val enc ie nn es 18 31 , but h ad a d et e rr en t eff ec t o n sc is sor ta il s erg ea n t
Abudefduf sexfasciatus (Lacépède 1831) and C.bennetti.
The barrier-reef sound attracted ve species (Apogon sp., C.striatus,D.aruanus,
R.aculeatus and S.microstoma) and repelled three others: C.citrinellus,clearn
squirrelsh Neoniphon argenteus (Valenciennes 1831) and blue gudgeon Ptereleotris
microlepsis (Bleeker 1856). Uncertainty on the attractive effect on C.brownriggii
remains as sh were found on the side where barrier-reef noise was played, but the
bay had repelled this species during the control-sound test.
The mangrove sound inuenced the distribution of seven species. Ctenochaetus stria-
tus and C.citrinellus were attracted, whereas narrowstripe cardinalsh Pristiapogon
exostigma (John & Starks 1906), P.fraenatus,N.argenteus,A.sexfasciatus and D.
aruanus were mainly found on the bay-sound side. As no attractive effect of bay sound
was previously shown by the control-sound test, the mangrove sound should deter them.
SYNTHESIS AND STRATEGY OF HABITAT SELECTION
Among the 20 species tested with white noise and habitats sounds, 16 reacted to at
least one sound, by being either attracted or repelled. Acanthurus triostegus,S.gua-
mensis,C.viridis and blueband goby Val en c i e nn ea s t r i g a ta (Broussonet 1782) did not
show any preferences or aversion for tested sounds.
The analysis of responses of individual species highlighted two selective strategies
in the choice of reef habitat: a directed selection of sound habitats (strategy A), or
the avoidance of some sound habitats (strategy B). In the avoidance choice, the sh
is repelled by a given sound and takes by default the remaining choice, whatever the
proposed sound. According to the behaviour observed during experiments, the strategy
was attributed to each species and its preferred habitat was rst putatively inferred
(Table I). This putative habitat was then compared with data from previous studies on
larval settlement in Moorea lagoon habitats (Lecchini & Galzin, 2003, 2005; Lecchini,
2005). Thirteen species have been found in at least one of the habitats predicted by
the analysis, suggesting the effective role of the sound in habitat selection. Predictions
could not be veried for three species (O.angustatus,S.spiniferum and C.citrinellus)
because their putative settlement habitats would be the bay and the mangrove, for which
surveys are currently lacking in Moorea.
Species from the same family did not most often react in the same way to the different
sounds. In other words, it is not possible to predict the choice of the family on the basis
of the behaviour of their species (Table I).
DISCUSSION
This study clearly demonstrates that different species within the same family respond
differently to broadcasted sounds. It highlights that studies dealing with the behaviour
of populations should consider the species level. Moreover, it is consistent with studies
showing that species within the same family settle in various habitats to decrease com-
petition (Sale, 1991; Rocha & Bowen, 2008; Lucy, 2010; Litsios et al.,2012;Bowen
et al.,2013).
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Biol ogy 2015, doi:10.1111/jfb.12651
REEF-SOUND INFLUENCE ON FISH LARVAE BEHAVIOUR 9
Three kinds of behaviour were observed. Firstly, four species (A.triostegus,V.stri-
gata,C.viridis and S.guamensis)didnotsignicantlyreacttoanysoundhabitat,
suggesting that sound may be an unimportant settlement cue for these species. Sec-
ondly, C.striatus was attracted by all the sounds, including the articial one, supporting
that this species may be attracted by any noisy areas. Thirdly, 15 other species were
either signicantly attracted by a single habitat sound (six species), repelled by one
or more sounds (seven species) or showed a combination (attraction and repulsion) of
both effects (two species).
Using different strategies for sound-based habitat selection support the initial ndings
of Radford et al. (2011) and Huijbers et al. (2012) concerning the effect of attrac-
tion. The shes use the acoustic cues to orientate during the settlement and are also
able to interpret the characteristics of the acoustic signals of the different habitats.
Avoidance of reef noise by pelagic crustacean larvae was described by (Simpson et al.,
2011), while a similar effect was described by Vail & McCormick (2011) for chemical
signatures of coral patches in Pomacentridae larvae. Here, sound will not only give
information on the attractiveness of a habitat, but also on appropriateness as a site for
settlement. Avoidance of inappropriate habitat sounds should consequently be included
in future studies.
On the basis of the experimental results, 65% of the tested species would select habi-
tats where they are usually found, validating the hypothesis that sound is used to select
their settlement habitats. Moreover, this percentage could be underestimated; the pre-
dicted habitat of O.angustatus,S.spiniferum and C.citrinellus were either the bay
or the mangrove but it is impossible to conrm it as these habitats were not surveyed
(Lecchini, 2005; Lecchini & Galzin, 2005). In the eld, some species are, however, also
found in habitats they would not select according to the present experiments. As shes
can also be attracted by visual (Lecchini, 2004; Igulu et al.,2011)andchemicalcues
(Sweatman, 1988; Atema et al.,2002;Lecchiniet al.,2005,2013;Vail&McCormick,
2011), the settlement choice is likely to be the result of the integration of all of these
signals over different spatial scales (Kingsford et al.,2002;Huijberset al.,2012).This
might explain why C.citrinellus and P.microlepsis are found on the barrier reefs in the
wild, although the sound of this habitat had a deterring effect on those species in this
study. It should also be borne in mind that the barrier reef has to be crossed to reach
other habitats (Irisson & Lecchini, 2008). Fishes might be found in this habitat because
they have not ended their settlement phase. It has been shown that coral-reef shes can
adopt a different set of settlement sequences: some can use a pre-settlement habitat or
can show a cryptic lifestyle, because larval morphology, physiology and diet are not
yet adapted to a reef habitat (Lecchini & Galzin, 2005).
Responses varied according to the type of sound, which clearly demonstrates the sen-
sory ability of larvae to select sounds that contain relevant information about habitat
types. This nding is corroborated by the fact that white noise had no effect on the
majority of the tested species, suggesting that noise per se is insufcient to elicit direc-
tional behaviour, as already shown in megalopae and cardinal shes larvae (Stanley
et al.,2011,2012;Holleset al.,2013).Thisstudydemonstratesthatthespectraland
temporal signature is important in elicited directional choices. Ostorhinchus angusta-
tus and S.spiniferum were attracted by bay sound, although the frequency richness of
this biotope is clearly not similar to that of other habitats (Fig. 1). The lack of spectral
complexity in the frequency range 1– 5 kHz may explain why the mangrove sounds
repelled ve species and attracted only one (C.citrinellus). These results are, however,
© 2015 The Fisheries Society of the British Isles, Journa l of Fish Bio logy 2015, doi:10.1111/jfb.12651
10 E. PARMENTIER ET AL.
intriguing as mangroves are known to be nursery areas for many species (Parrish, 1989;
Nagelkerken et al.,2000;CocheretdelaMorinièreet al.,2002;Nagelkerkenet al.,
2002). The mangrove habitat in Moorea is almost silent, with sparse clicks. The mod-
ications applied to the mangrove soundtracks (increasing the click rate by skipping
the silent parts) might have altered the sonic information of this habitat.
This study showed that most of the coral-reef sh species tested use sounds to detect
and orientate towards appropriate habitats at settlement. Based on observations, two
kinds of strategies can be attributed to larva behaviour: a direct selection for sound
of appropriate habitats, or avoidance of inappropriate habitats, and thus preference by
default for the other ones. Moreover, the strategy used and the habitat chosen varied
between species within families, highlighting the importance of conducting studies on
sound inuences on behaviour at the species level. Coastal habitat noise heterogeneity
appears to be used adaptively by the different sh species.
The authors thank the team of the Centre de Recherches Insulaires et Observatoire de
l’Environement (CRIOBE) for their assistance and logistical support during the study. E. Fors-
gren and anonymous referees made constructive comments on the manuscript. This research
was supported by the Fonds de la Recherche Scientique (FNRS), an EPSRC studentship
and Subacoustech funding to S.N., and Defra (Contract ME5207) and NERC (KE Fellowship
NE/J500616/1) to S.D.S.
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Environmental fundamentals like time, senses, and signs originate as many ecoscapes (timing-scapes, sensory-scapes, semio-scapes) species specific. Timing-scape is represented by a mosaic of patches shaped by phenomena that occur at a geological, biological, ecological, cultural, and semiotic time.
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