The Behavioural Response of Coral Reef Fish Following Introduction to a Novel Aquarium ...

26 Pages·1980·0.44 MB·English

The behavioural response of coral reef fish following
introduction to a novel aquarium environment
ANDREWB.GILLandMARKJ.ANDREWS
JonesBuilding,SchoolofBiologicalSciences,UniversityofLiverpool,P.O.Box147,Liverpool,
L693BX,UK
Received9September2000,acceptedinrevisedform11September2001
Keywords:reeffish,novelenvironment,locomotorymode,activity,behaviour
ABSTRACT
Followingtheconstructionofalarge-scalepublicaquarium,wewerepresentedwithanopportu-
nitytoinvestigatehowwildcaughtCaribbeanreeffishrespondtotheirfirstencounterwithanovel
environment.Withintheconstraintsofthisopportunity,wedesignedabehaviouralstudytodeter-
minethereeffishes’responsetoanewhabitatinrelationtotheirlocomotorymode.Ninespecies
offishrepresentingthreelocomotorymodes:carangiform,sub-carangiformandlabriform/sub-
carangiformwereobservedoverafour-weekperiodfollowingtheirfirstintroductiontotheaquar-
ium.Fishactivitylevelsandspatialdistributionwerequantifiedinrelationtotimesincetheirfirst
encounterwiththenovelenvironment.Themostimportantresultwasthat,regardlessoflocomo-
torymodeorecology,allofthespeciesextensivelyexploredthenovelenvironmentratherthan
settleonthefirsthabitatthattheyencountered.Thisisaparticularlyinterestingresultforterritorial
species.Morespecifically,however,thereweresignificantdifferencesbetweenspeciesinactivity
throughtime.Carangiformactivitylevelwaslowestintheinitialphasesofanencounterwiththe
novelenvironmentsubsequentlyrisingtoastablelevel.Theotherspecieshadvariableactivity
throughoutthestudy,butallofthemexhibitedaphaseoflowactivityatsomestageduringthe
study.Intermsofthefishes’useofthe2.5millionlitresofwater,sixspeciesutilisedthewhole
oftheaquariumbasedonapredefinedzoningscheme.Althoughtheinitialactivitylevelwaslow,
carangiformswimmersusedatleast90%ofthezonesintheearlyphasesofanencounterwith
thenovelenvironmentandsubsequentlyusedallofthezones.Sub-carangiformspeciesalsoused
100%ofthezonesbytheendofthestudy.Threeofthefourlabriform/sub-carangiformswimmers
usedamaximumof90%ofthezones.Therewasnosignificantdifferencebetweenspeciesintheir
useofthezones.However,eachindividualzonewassubjecttodifferentialusebythefish.Owing
to the extensive scale of the aquarium, we discuss the applicability of the behavioural results
obtainedtothenaturalenvironmentinthecontextoftheecologyofthespeciesoffishstudied.
INTRODUCTION
Thewayinwhichafishutilisesagivenhabitatdeterminesitsacquisitionoffood,
refugeorterritory.Morespecifically,thedifferentialabilityofeachspeciesoffish
to exploit a given resource is a function of their ecomorphological relationships
(Mottaetal,1995)suchasbodysize(GillandHart1994,1996;Aburto-Oropeza
etal.,2000)andlocomotoryability(Webb,1984;Webbetal.,1996)inrelationto
theavailableresources.Coupledwiththesefunctionalconstraintsisthedynamic
abilitytorespondtoresourceopportunities,whichvaryonaspatialandtemporal
basis(Letourneur,2000),whichwillalsobeinfluencedbythelearningabilitiesof
thefish(CroyandHughes,1991a).Hence,thebehaviouroffishstudiedwithina
givenhabitatwillbeaconsequenceofacombinationofthesefactors.
AquariumSciencesandConservation3:281–306,2001.
©2001KluwerAcademicPublishers.PrintedintheNetherlands.
282 A.B. GILL ANDM.J. ANDREWS
In the natural environment, we observe fish at a particular point in their life
whereweassumetheyhaveexperience,andtherefore,somepriorknowledgeofthe
environmentaroundthem.Inessence,wetakeasnapshotlookataparticularperiod
duringtheirlifewithintheirchosenhabitat.Onepotentiallyimportantconceptthat
isdifficulttoquantifyatpresentishowthefishwouldreacttoanovelenvironment
about which they have no prior experience. We see an example of this during
recruitmenttoacoralreefwheretheabilityoffishlarvaetodiscriminatebetween
habitats is crucial for post settlement survival owing to the species-specific and
individualrequirements(Eckert,1987;Doherty,1991).Thefunctionalandlearning
abilitiesofanewlysettledfishwillinfluencetheoutcomeofthisinitialperiodofan
encounterwiththenovelenvironment.However,thisisnottheonlytimeinthelife
cyclewhereafishmayencountersurroundingsdifferenttothosetowhichitwas
previouslyexposed.Followingnatural(e.g.hurricane,volcanic)oranthropogenic
(e.g.dynamite)perturbations,adultfisharelikelytoencounteravastlychanged
topographyandresourceavailability.Insituationsofthisnature,theresponseofthe
adultfishwillalsobeinfluencedbytheirabilitytolearnaboutthenewenvironment
andtheirfunctionalcapabilities.Inaddition,theirspecificresourcerequirements
andtheexistenceofotherspeciescompetingforsimilarresourceswillshapethe
resettlementprocess.
Inthiscontext,aquariumscanrepresentachangeofhabitatandresourceswhen
fisharefirstintroduced.Themoderndaypublicaquariumaimstoprovidearep-
resentative display of the natural environment and the scale of some are large
enoughtoprovideanarrayofhabitatopportunitiesreadyforexploitationbythe
fishfollowingfirstintroduction.
TheBluePlanetAquarium,builtinEllesmerePort,Cheshire,UKwasopened
inJuly1998.Priortoitsopeningtothepublic,anopportunityarosetoinvestigate
differentCaribbeanreeffishspeciesfromfirstintroductiontothemainaquarium
exhibit.Inordertotakeadvantageofthisopportunity,wehadtoworkwithinthe
scheduleoftheaquariumstaffwhichwasdeterminedbythearrivaldatesandaccli-
matisationofthefish.Withtheseconstraintsinmind,wedesignedabehavioural
ecologystudythatwouldincreaseourunderstandingofhowthedifferentspecies
ofreeffishrespondedtoexposuretoanovelenvironmentinrelationtotheirloco-
motoryclassification.
Although this is not a common occurrence, data obtained from such studies
provideanopportunitytodeterminehowfishreactwhenintroducedtoanaquarium,
representingacontrolledenvironment,andprovidepossiblecorrelateswithdata
basedonfishresponsestonewopportunitiesarisingthroughsucheventsashabitat
displacementwithintheirnaturalenvironment.
The principal aim of the study, therefore, was to investigate species-specific
behavioural response to a novel environment in relation to time since a first
encounter.Weassumedthat,ingeneral,therateoflearningbythefishwouldbe
amajorfactorimmediatelyonanencounterwiththenewenvironment(Hughes,
1997)andduringthesubsequentdays,decliningtoastablelevelafter5–7days,
as has previously been shown for laboratory studies on fish learning related to
BEHAVIOUR IN A NOVEL ENVIRONMENT 283
foraging by Croy and Hughes (1991a). We hypothesised that, during this period
oflearning,differentspecieswouldreacttoanewhabitatopportunityaccording
totheirfunctionalcapabilitiessuchaslocomotorymodeandalsotheirecological
determinants. This would likely have a bearing on the exploratory behaviour of
thefishandwouldbemanifestbydifferentialuseofthenewenvironment.Hence,
wepredictedthatspatialactivitywouldbeafunctionofboththerateoflearning
andthelocomotoryabilityofthespecies.
METHODS
Allobservationstookplacebetween13Juneand7July1998attheBluePlanet
Aquarium, Ellesmere Port, UK. The focus for the study was the main exhibit
tankmeasuring34m×26m×5m(approx.)andcontaining2,500,000Lofwater
maintainedat22◦Cand32%salinity(Figure1).Theaquariumdisplay,constructed
entirely of cement, simulated a coral patch reef environment and was consistent
withstructurescommontothistypeofcoralreef(includingmassiveandbranching
hardcoralsandsponges;pers.obs.).Wherethebottomofthetankwasnotpartof
thecoralreefstructure,itwaseitherasandorhardsubstratum.Illuminationfrom
above the water provided a 12:12h light:dark regime. Light levels, in units of
µEm−2s−1weremeasuredthreetimesatthecentralpointofeachdefinedzoneof
thetank(Figure1)usingasubmersibleMacamQ102radiometerwithanSD101Q
Cossealeddetector.Watermovementwasalsomeasuredthreetimesatthecentral
pointofeachzonewithacurrentmeter(Z210,A.Ott,Kempten).
Allfishwerecollectedbyconventionaltechniques(netorline)alongthecoast
ofFlorida,USA.Followingstandardtransportationmethods,thefisharrivedatthe
aquariumaminimumof13haftercapture.Followinganacclimationperiod,which
lastedapproximately1hwithinafeatureless,circularquarantinetank,thefishwere
introducedintothemaintankthroughanaccessgate(Figure1).Throughoutthe
study period, food was haphazardly distributed by hand from the above water
walkwaythreetimesaday,behaviouralobservationswerenevermadeduringor
aroundfeedingtimes.
Ninespeciesoffishwereselectedfromthe15speciesintroduced,torepresent
arangeoflocomotorytypes(asdefinedbyBlake,1983)andineachcase,atleast
twoexamplesofaparticulartypewerestudied(Table1).Allthefishwereadultsin
multiplespeciesgroups(Table1)exceptforPomacanthusparuwhichwasrepre-
sentedbytwoadvancedintermediatespecimens.Selenevomer,Caranxlatusand
Alectisciliariswereselectedtorepresentcarangiformswimmersthatprincipally
usetheircaudalfinasapropulsiveforceandconfineundulationsofthebodytothe
posteriorthirdofthebody(Blake,1983).Thisformofpropulsionrequiresahigh
aspectratiofinandisusedbypelagicfishforsustainedswimming.Inaprogression
towardspropulsionwithagreaterinvolvementoftheanteriorofthebody,Lutjanus
griseusandOcyuruschrysuruswereselectedassub-carangiformswimmers.Sub-
carangiform fish are characterised by a highly flexible, low aspect ratio caudal
284 A.B. GILL ANDM.J. ANDREWS
Figure1. Planviewofthemainexhibittank,BluePlanetAquariumincorporatingthegridsystem
(zonesA1–D3)usedtodivideupthetankforobservationaldatacollection.Key:LL=meanlight
levelµEm−2s−1;%S=estimateofthe%ofzoneareacontainingnostructures,overhangsor
tunnel. = Submergedoverhangssurfaceto0.5m; = Submergedcoralreefformations;
= Sandysubstratum; = Hardsubstratum; = Abovewaterconcreteplatform;(cid:1)=Metal
Supportingstructure; = viewingwindow;∗=AccessGate(Allspeciesintroducedfromthis
point);−·−·=Positionofabovewaterwalkwaysandzoneboundaries;---=6mdeepsection,
theremainderofthetankwas3.5–5mdeep.
BEHAVIOUR IN A NOVEL ENVIRONMENT 285
mingoural n 785768578
mvi m mmm
mduringstudy.Theswin=n.numberofbeha wimmingmode arangiformarangiformarangiformubcarangiformabriform/Sub-carangiforubcarangiformabriform/Sub-carangiforabriform/Sub-carangiforabriform/Sub-carangifor
ariugive S CCCSLSLLL
naqunsis ated
individualsiIobservatio PhaseIiniti OnreleaseOnreleaseOnreleaseWithin12hWithin12hOnreleaseWithin12hOnreleaseOnrelease
ofse
berPha no.
umof Max 6053 +0+01
nn 231125516
bservedandmaximumenreleaseandinitiatio Commonname AfricanPompanoLookdownsHorse-eyeJackGraySnapperFrenchAngelYellowtailSnapperPorkfishSergeantMajorBluestripedGrunt
oe
w
Table1.Listofspeciesmodeandthetimebetobservations Species AlectisciliarisSelenevomerCaranxlatusLutjanusgriseusPomacanthusparuOcyuruschrysurusAnisotremusvirginicusAbudefdufsaxatilisHaemulonsciurus
286 A.B. GILL ANDM.J. ANDREWS
fin, making them better suited to rapid acceleration than steady swimming. The
remainingfourspeciesoffishwereselectedfortheiruseofboththelabriformand
thesub-carangiformswimmingtypes.Haemulonsciurus,Anisotremusvirginicus,
AbudefdufsaxatilisandP.paruusetheirpectoralfinsforpropulsionwhenmoving
slowly over short distances. These labriform swimmers shift to sub-carangiform
locomotion if acceleration or sustained swimming is required (Helfman et al.,
1997;pers.obs.).
Throughoutthisstudy,weconsideredtheeffectoftimefollowingintroductionto
anovelenvironmenttobeaninfluenceonthespatialactivityoftheninespeciesof
Caribbeanreefteleosts.Therefore,twomajoraspectsoftheactivityofeachspecies
offishwereexaminedinrelationtotime:(1)theleveloflocomotoryactivity;and
(2)spatialdistribution.
Visualobservationsweremadefromtheabovewaterwalkwaysapproximately
2m from the water surface (Figure 1). All observations took place before the
aquarium was open to the public, and any potential for disturbance by staff
and labourers working around the aquarium was considered to be negligible
as no fish were seen to react during the studies. Owing to some restrictions
in accessibility to the aquarium and differences in the arrival dates and times
of species, our observations were made on an opportunistic basis. The time
of day when a species was observed was between 10a.m. and 1p.m. each
studyday.
Forallvisualobservationsthetankwasdividedinto10zonesofapproximately
equalsizedelineatedbytheabovewaterwalkways(Figure1).Zoneswerelabelled
on a grid system from A1–D3 (Figure 1). Observations were made within two
distincttimeperiods.Firstly,aseriesofbetweenthreeandeightobservationswere
madeforeachspeciesbetween13thand24thJune1998.Thesewereinitiatedeither
from the moment of introduction to the new environment (six species; Table 1)
orwithinthefirst12h(threespecieswhicharrivedduringthenightpriortotheir
first observation; Table 1), and referred to as Day 1 in the subsequent analysis.
Inadditiontotheninespeciesstudied,therewereotherspeciesofteleostpresent
duringtheobservationperiods(Table2).Secondly,asinglefinalobservationwas
madeforeachoftheninespeciesonthe6thor7thJuly1998.Atthisstage,there
were a total of 15 different species in the tanks (Table 2) all of which had been
presentsince25thJune1998.
To investigate the effect of exposure to a novel environment on the relative
activitylevelsofeachspeciesovertime,afocalfishwaschosenatrandomfroma
speciesgroupandsampledinstantaneouslyat30sintervalsforaperiodof15min.
Ateachsamplepointwerecordedinseriesthezoneinwhichthefocalfishwas
located. Any fish observed on a boundary between zones was recorded as being
inthezonenextvisited.Theleveloflocomotoryactivityofthefishwastherefore
definedwithineach30sintervalaccordingtothreecategories:
Type0=remainedwithinaparticularzone
Type1=movedtoanadjacentzone
Type2=movedthroughoneormorezones
BEHAVIOUR IN A NOVEL ENVIRONMENT 287
Table2. Listofadditionalspeciespresentintheaquariumandthenumber
ofindividualsofeachspecies.Thepresenceofeachspeciesinrelationtothe
phaseofthestudyisgiven
Species Commonname Maxno. Phasepresent
Holocentrusascensionis Squirrelfish 2 I,II,III,IV
Carangoidescrysos Bluerunner 50+ III,IV
Epinephelusguttatus RedHind 2 II,III,IV
Diodonhistrix Porcupinefish 2 I,II,III,IV
Balistesvetula QueenTriggerfish 3 II,III,IV
Carchariastaurus SandTigerShark 4 IV
The fish had no individual identifiable markings; therefore, on each sampling
occasion we chose any one individual fish from a group of the target species
andfolloweditforthedurationofthesamplingperiod.Werecordedwhetherthe
focalfishremainedwiththeotherfishinthegroupthroughoutthesampleperiod.
H.sciurusandA.saxatilisweretreatedassinglefishobservations,astheytended
to be solitary or form very loose small aggregations. In addition, we noted any
interactions of the focal fish with other fish sharing the vast aquarium. During
17% of observations, the focal fish disappeared from the view of the observer
andthesamplingwasprematurelyterminated.Thiswastakenintoaccountinthe
subsequentanalysisbystandardisingthesampletime.
Based on the principle that the rate of learning in fish decreases significantly
from Day 1 reaching a constant level after around five days (Croy and Hughes,
1991a,b)wedividedtherecordingofdataintophasesaccordingtothetimesince
introduction:
PhaseI(Day1)—thena¨ıveperiodowingtonopreviousexperience
PhaseII(Day2–4)—theperiodwhenthefishshowadramaticchangeinlearning
Phase III (Day 5–13)—the period where the learning has reached a constant
level
PhaseIV(Day18+)—thefinalrecordforaspecies,10+daysafterPhaseIII.
The data did not meet the assumptions of parametric statistics (Siegel and
Castellan,1988)andwerethereforeanalysedusingthenon-parametrictests,χ2and
FriedmanANOVA(withmultiplecomparisoncalculatedmanuallywithreference
to Siegel and Castellan (1988)). All analyses were undertaken with the SPSS
software.
RESULTS
Where a focal fish was a member of a group, it remained with the other shoal
membersfor91%oftheobservationsthroughouttheobservationalsampleperiod,
hencetheactivityofanyonefocalfishcloselymatchedthatoftheotherindividuals
oftheshoalingtargetspecies.Therewasalowlevelofinteractionrecordedbetween
288 A.B. GILL ANDM.J. ANDREWS
thefishspeciesinthetank(33occasionsfrom1560records)withonly5records
of aggression. The few interactions observed were occasional mixing of shoals
and inspection behaviour particularly when a species was first introduced to the
aquarium.
Inter-specificactivity
Significantdifferencesinactivitylevelswereobservedamongspecies(Friedman
ANOVA, χ2 = 18.667, df=8, p = 0.017) with the carangiform fish being the
most active followed by the sub-carangiform and then the labriform swimmers
(Figure2).FollowingFriedmanANOVAmultiplecomparisontestingAlectiscil-
iaris was shown to have a significantly greater level of activity than H. sciu-
rus, O. chrysurus, P. paru, A. virginicus, and A. saxitilis (|R − R | ≥ 15.18
u v
at p = 0.05). Whereas, H. sciurus had significantly lower activity levels than
A. ciliaris, S. vomer, C. latus and L. griseus (|R − R | ≥ 15.18). We there-
u v
forecategorisedthespeciesintotwogroupsbasedontheiractivityrelativetothe
most and least active species: Group 1: active species; and Group 2: low activ-
ityspecies(Figure2).Group1consistedofthethreecarangiformandoneofthe
sub-carangiformspecies(A.ciliaris,S.vomer,C.latus andL.griseus).Group2
was represented by the other species of sub-carangiform (O. chrysurus) and the
labriform/sub-carangiform swimmers (H. sciurus, P. paru, A. virginicus, and A.
saxatilis).Therewerenosignificantdifferencebetweentheoverallactivitylevels
offishclassifiedwithinthesamelocomotorygroup(FriedmanANOVAmultiple
comparisons|R −R |≤15.18).
u v
Relative activity/day
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Alectis ciliaris
Selene vomer
Caranx latus
Lutjanus griseus
Pomacanthus paru
Ocyurus chrysurus
Anisotremus virginicus
Abudefduf saxatilis
Haemulon sciurus
Figure2. Medianrelativeactivityperday(including10thand90thpercentiles).Specieshave
beendividedintotwogroups;Where = Group1;and(cid:2)= Group2(seetextfordetails).
BEHAVIOUR IN A NOVEL ENVIRONMENT 289
Table3. Statisticallysignificantchanges(p < 0.05)inactivitywithinandbetweenthe
differentPhasesbasedondatainFigure4.(seetextfordetailsofPhases)
Species PhasesIandII PhaseIII FromPhaseIIItoIV
Alectisciliaris Increase Stable Stable
Selenevomer Increase Decrease Stable
Caranxlatus Increase Stable Stable
Lutjanusgriseus Stable Decrease+increase Decrease
Pomacanthusparu Stable Stable Decrease
Ocyuruschrysurus Increase Decrease Increase
Anisotremusvirginicus Stable decrease stable
Abudefdufsaxatilis Decrease decrease stable
Haemulonsciurus Increase decrease increase
Individualspeciesactivity
Whenconsideringobservationsintheirtemporalsequence(PhaseI–IV)through
the study a number of significant changes in activity occurred and these were
analysed in relation to the locomotory mode of the fish. Over the course of
the various Phases of the study, some species exhibited stable activity levels,
notably the carangiform swimmers (Table 3; Figure 3(a–c) while other species
showed variable levels of activity (Table 3, Figure 3). All the species showed
some degree of low activity (Type 0) during the observational period with the
carangiform swimmers having the lowest activity during Phase I and all other
species in the latter Phases (Figure 3). During Phases I and II, five species sig-
nificantly increased their activity (S. vomer χ2 = 24.36,df =1,p < 0.001; C.
latusχ2 =15.92,df =1,p <0.001;A.ciliarisχ2 =15.14,df =1,p <0.001;
O.chrysurusχ2 = 6.36,df = 1,p = 0.01;H.sciurusχ2 = 8.78,df = 1,p =
0.003;Table2),threespeciesdidnotsignificantlychangeactivitylevel(L.griseus
χ2 = 3.45,df =1,p > 0.06; A. virginicus χ2 = 1.38,df =1,p = 0.24; P.
paru χ2 = 0.67,df = 1,p = 0.41; Table 3) and a single species, A. saxitilis,
significantlyreducedactivity(χ2 =4.88,df =1,p =0.03;Table3).
Carangiformswimmers
Whenconsideringallthefishspeciesstudied,thiscategoryofswimmersutilised
thegreatestamountofType2activity.Twoofthethreespeciesclassifiedascarangi-
form swimmers, C. latus and A. ciliaris, had a similar pattern of activity (Table
2,Figure3a,c).DuringPhasesIandIItheiractivityincreasedreachingaconstant
levelfortheremainderofthestudy.(PhasesIIIandIV,C.latusallχ2 <1.71,df =
1,p > 0.18; A. ciliaris all χ2 < 2.47,df = 1,p > 0.12). The other species in
thiscategory,S.vomer,wassimilarinitsoverallpatterntotheothertwospecies
butwithgreatervariabilityinactivitylevel(Figure3b).Thisspeciesexhibitedthe
same initial increase in activity between Phases I and II, however, during Phase
IIactivityatfirstreduced(χ2 = 5.68,df = 1,p = 0.02)butthensubsequently
increased(χ2 = 21.79,df = 1,p < 0.001;Figure3b).ThroughoutPhaseIII,S.
290 A.B. GILL ANDM.J. ANDREWS
Figure3. TherelativefrequencyofActivity,Parts(a),(b),and(c).