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Ecological
Indicators
jou rn al h om ep a g e :w w w . e l s e v i e r . c o m / l o c a t e / e c o l i n d
Indicators
of
movement
and
space
use
for
two
co-occurring
invasive
crayfish
species
P.M.
Anastácio
a,∗,
F.
Banha
a,
C.
Capinha
b,
J.M.
Bernardo
c,
A.M.
Costa
c,
A.
Teixeira
d,
S.
Bruxelas
eaMARE–MarineandEnvironmentalSciencesCentre,DepartamentodePaisagem,AmbienteeOrdenamento,EscoladeCiênciaseTecnologia,
UniversidadedeÉvora,RuaRomãoRamalho59,7000-671Évora,Portugal
bCIBIO/InBio,CampusAgráriodeVairão,RuaPadreArmandoQuintasn◦7,4485-661Vairão,Portugal
cDepartamentodePaisagem,AmbienteeOrdenamento,EscoladeCiênciaseTecnologia,UniversidadedeÉvora,RuaRomãoRamalho59,
7000-671Évora,Portugal
dCIMO-ESA-IPB,MountainResearchCentre,SchoolofAgriculture,PolytechnicInstituteofBraganc¸a,CampusdeStaApolónia,Apartado1172,
5300-855Braganc¸a,Portugal
eInstitutodaConservac¸ãodaNaturezaedasFlorestas,I.P.,AvenidadaRepública16,1050-191Lisboa,Portugal
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received12June2014 Receivedinrevisedform 23December2014 Accepted9January2015 Keywords: Radio-tracking Biologicalinvasions Dispersal IberianPeninsula River Crustacea
a
b
s
t
r
a
c
t
Redswampcrayfish(Procambarusclarkii)andsignalcrayfish(Pacifastacusleniusculus)aretwoinvasive freshwaterspecieswithaworldwidedistribution.Theobjectiveofthisworkwastoinvestigatehowthe twospeciesmoveandusespaceinanareaofrecentcoexistence.Simultaneously,wetesttheuseof newtoolsandindicestodescribetheirmovementpatterns.Toaccomplishthisweperformeda radio-trackingprogramwithinariver-typehabitatduringtwodifferentperiods(September/October2010and June/July2013).Weusedspatialanalysistoolstomapcrayfishradio-locationdatawithandwithout accountingforthecurvatureoftheriver.Toassesstheconsistencyofthedirectionofmovementandof thedistancestraveledbycrayfish,twoindicesweredeveloped.Toassessthehabitatpreferencesofeach speciesweappliedIvlev’sElectivityIndexandtheStandardizedForageRatio.MovementofP.clarkiiand P.leniusculusdiffered.Theaveragedetectedmovementwas8.8mday−1forP.clarkiiand17.5mday−1for
P.leniusculus.However,crayfishbehaviorrangedfromalmostcompleteimmobility–sometimesduring severaldays–tolargemovements,inhalfaday,uptoamaximumof255mforP.clarkiiand461mfor P.leniusculus.Theproportionofupstreamordownstreammovementswasindependentofthespecies andbothspeciesdisplayednopreferenceforeitherdirection.Theindicesofconsistencyofmovement showedalargeinterindividualvariation.Speciesandperiod(2010or2013)affectedthemeandaily distancetraveled,maximumobserveddistancefromlocationofreleaseandpercentageofobservations undervegetationcover.TheIvlev’sElectivityIndexandtheStandardizedForageRatiopresentedsimilar results.P.clarkiishowedapreferenceforpoolareaswithriparianvegetationcoverwhileP.leniusculus preferredriffleandpoolareaswithriparianvegetationcover.Ourworkprovidednewandvaluabledata formodelingtheactivedispersalofthesetwoproblematicinvadersinacontextofcoexistence.
©2015ElsevierLtd.Allrightsreserved.
∗ Correspondingauthor:MARE–MarineandEnvironmentalSciencesCentre, DepartamentodePaisagem,AmbienteeOrdenamento,EscoladeCiênciase Tec-nologia,UniversidadedeÉvora,RuaRomãoRamalho59,7000-671Évora,Portugal. Tel.:+351266745385.
E-mailaddresses:anast@uevora.pt(P.M.Anastácio),filipebanha@hotmail.com
(F.Banha),cesarcapinha@outlook.com(C.Capinha),jmb@uevora.pt(J.M.Bernardo),
amac@uevora.pt(A.M.Costa),amilt@ipb.pt(A.Teixeira),Sofia.Bruxelas@icnf.pt
(S.Bruxelas).
1. Introduction
Duetotheireconomicvalue,severalspeciesofcrayfishwere
introducedoutside their nativeranges.Unfortunatelythere are
numerous freshwatercrayfish speciesbecoming invasivein the
areasofintroduction(Holdich,1988;HenttonenandHuner,1999;
Gherardi,2013)andthetwomajorexamplesaretheredswamp
crayfish (Procambarus clarkii)and the signalcrayfish
(Pacifasta-cusleniusculus).Bothspeciesnowhaveverylargeinvasiveranges
worldwide and furtherspread is expected since there are still
wideareasoftheplanetwithadequateenvironmentalconditions
(Capinhaetal.,2011).
http://dx.doi.org/10.1016/j.ecolind.2015.01.019
Fig.1. Locationofthestudyarea.ThegrayareahighlightedbyanarrowindicatestheregionwithinthePortugueseterritorycoveredbythelargermap.Theredmarksignaled bytheletter“a”markstheradio-trackingareawithintheriverMac¸ãs.(Forinterpretationofthereferencestocolorinthistext,thereaderisreferredtothewebversionof thearticle.)
Theredswampcrayfishisnativetosubtropicalregionsof
north-easternMexicoandsouth-centralUSA.Thisspecieshasahighly
plasticreproductivecycle(Gherardi,2006)andawideecological
plasticity(Gherardi,2006;Souty-Grossetetal.,2006)andcurrently
itisthemostwidelyintroducedcrayfishintheworld(Gherardi,
2006).InEuropethespecieswasfirstintroducedin1973in
south-ernSpain(Habsburgo-Lorena,1978)anditrapidlyspreadacross
severalEuropeancountries(Laurent,1997; Souty-Grossetetal.,
2006)showingthewidestinvasiverangeforanaliencrayfish.
Thesignalcrayfishisnativefromthecooltemperateregions
ofWesternNorth America and it isendemic toWesternNorth
AmericabetweenthePacificOceanandtheRockyMountains.Its
habitatrangesfromlotictolenticsystemsbutitisableto
toler-ateexposuretobrackishwater(LoweryandHoldich,1988;Lewis,
2002).P.leniusculuswasfirstintroduced tonorthern Europein
the1960storeplacedecreasingstocksofthenativeAstacus
asta-cus(Abrahamsson, 1973;Westman, 1973).Currently this isthe
mostwidespreadinvasivecrayfishinEurope,beingpresentin27
countries(Holdichetal.,2010).
Invasive crayfish affect not only the distribution of native
crayfishbutalsothedynamicsandbiodiversityoftheinvaded
com-munity(GherardiandHoldich,1999;Gherardi,2006;Holdichetal.,
2010).BothP.clarkiiandP.leniusculusareresponsiblefor
multi-plenegativeimpactsonnativespecies,ecosystemsandeconomic
activitiesinthenewranges.However,thesenewarrivalsincreased
thecommercialvalueofcrayfishinEuropeandinmanyotherparts
oftheworld(Nyström,1999;Souty-Grossetetal.,2006).
Onamacroscale,humanintroductionsandenvironmental
suit-abilitycan successfullyexplain thedistributionof P.clarkii and
P.leniusculusinEurope(Capinhaetal.,2013).However,thelocal
spreadandprogressionoftheinvasionfrontswithinorevenacross
countrybordersneedstobeaddressedifmitigation,management
orcontainment actionsaretobeimplemented. Severalauthors
studiedtheprogressionoftheinvasionfrontorthemovement
pat-ternsofeachofthesespecies(e.g.Bubbetal.,2004;Aquilonietal.,
2005;Kerbyetal.,2005;Bernardoetal.,2011;Almeidaetal.,2013; Johnsonetal.,2014)butnotthecoexistenceofthetwospecies.P.
environmentalniches(CapinhaandAnastácio,2011).Aseachof
thesespeciesexpandsitsinvasiverange,theareasofcoexistence
becamewiderandthereforesomeinteractionsmayoccur,
poten-tiallyaffectingthepatternsofspaceuseandspeedoftheinvasion
front.Infact,withintheIberianPeninsula,therearealreadysome
areasofcoexistenceofbothspeciesandsomeeffortisbeing
con-ductedtodocumentonaregionalscalehowthespreadofthese
twospeciesisaffectedbythiscoexistence(Bernardoetal.,2011).
Thereareseveralsoftwaretoolsforanalyzingmovementand
spacedistributionofterrestrialspeciesthatprocessdatacollected
byradio-tracking.However,riversystemshavealinearstructure
andarethereforeinadequatelyapproachedbysomeofthesetools.
Oneoftheproblemsisthedeficientcalculusofthedistanceswhen
ariverhasastronglycurvilinearshape.Anotherdifficultyconcerns
themostlytwo-waydirectionalityofthemovement.Ourobjective
istofindouthowthetwoinvadersmoveandusespaceinanarea
ofrecentcoexistencewhilesimultaneouslytestingtheuseofnew
indicesfordescribingthepatternsofmovementinriversystems.
2. Methods
DuringthemonthsofSeptember/October2010andJune/July
2013aradio-trackingprogramwasundertakenwithinashallow
1330mstretch oftheriverMac¸ãs, Trás-os-Montes,NEPortugal
(Fig.1),betweentwoadjacentsmalldams.Thisstretchhasa
rel-ativelyrecentpopulationofboththeredswampcrayfishandthe
signalcrayfish(Bernardoetal.,2011).
2.1. Mesohabitatmapping
River shape, mesohabitat types and vegetation cover were
mapped(Fig.2)bycombiningdetailedinsitucartographic
mea-surementswithaerialimagery(1mresolution)availablefromthe
software ArcMap10.1. Vegetation cover wasmappedas
“pres-ence”or“absence”andreferredtoripariancanopyortoanykind
ofemergentvegetation.Thisincludedtrees,shrubs andaquatic
macrophytes, without species identification. Water speed was
measured using the float method (Meals and Dressing, 2008).
Mesohabitatswereclassifiedaspools,rifflesandrunsaccording
tocurrentvelocityandturbulence,whichwasvisuallyassessed.
CorrespondenceoftheobservedmesohabitattypestoNewsonand
Newson(2000)surface flow types is asfollows. Pools:no
per-ceptibleflow,smoothsurface,reflectionswithnoorveryminor
distortion; Runs: smooth boundary turbulent flow (very little
surface turbulence, very small turbulent flow cells are visible,
reflectionsaredistorted);Riffles:rippledflow(watersurfacehas
regulardisturbances,whichformlowtransverseripplesacrossthe
directionofflow),brokenstandingwaves(standingwavespresent
whichbreakatthecrestoriginatingwhitewaters),chuteflow(fast
flowoverbouldersandbedrock).Poolshadameanspeedofzero
(i.e.undetectedmovement),runshadameanspeedof0.05ms−1
andrifflespresentedameanspeedof0.25ms−1 andturbulence
causedbytheroughnessofthestreambed,slopeandshallowdepth.
Sixhabitattypesweredefinedbasedonthecombinationsof
meso-habitatandvegetationcovertypes:Poolwithoutcover,Poolwith
cover,Runwithoutcover,Runwithcover,Rifflewithoutcoverand,
Rifflewithcover.
2.2. Radiotrackingprocedures
Tracking wasperformed in two periods:September/October
2010(4P.clarkiiand8P.leniusculus)andJune/July2013(3P.clarkii
and4P.leniusculus).Bothspecieswereactiveduringtheseperiods
oftheyearandaveragewaterdepthwasenoughforcrayfish
move-mentandnottoodeepforradio-trackingalongthewholeriver
Fig.2.Vegetationcoverandturbulencemapsofthestudiedriverstretch.Pools hadameanspeedofzero(i.e.undetectedmovement),runshadameanspeedof 0.05ms−1andrifflespresentedameanspeedof0.25ms−1andturbulence.
sector. Additionally, during these periods, mesohabitat
hetero-geneitywaslargeandhabitatswereaccessibletotheradio-tracking
teammovingalongtheriver.P.leniusculustotallengthrangedfrom
7.7to10.9cm(mean=9.76cm)andP.clarkiitotallengthranged
from9to10.5cm(mean=9.78cm).In2010weusedTelenax
trans-mittersmodelTXB-004G–150MHzwithon–offmagneticswitch
(1.2g,0.7cm×0.8cm×1.3cm)andin2013weusedBiotrack
trans-mitters (PIP2 single celled tags, with medium potting). Signal
receptionwasassuredwitha3elementfoldableYaggitypeantenna
andaRX-TLNXreceiver(bothsuppliedbyTelenax).Crayfishwere
trackedtwiceaday,atsunriseandsunset,witha10–30cmradius
precisionfor a period of 6–30 days (mean=21 days;S.E.=1.6),
dependingonbattery lifeandpredationupon crayfish.The
dis-tancetothelastposition,movementdirectionanddistancetoeach
marginoftheriverweremeasured.Additionally,eachpositionin
theriverwasregisteredbyaGPSdevice(Garmin,modelOregon
550t).Waterdepthand habitattypewererecordedwhenevera
crayfishwaslocated.Duringeachradio-trackingsessionwater
vari-ablesweremeasuredwithaWTWMultilineF-set.In2010,mean
watertemperaturewas20.4◦C(SD±1.8),meanpHwas7.3(SD
±0.3),meanconductivitywas148.1S/cm−1(SD±14.3)andmean
dissolvedoxygenwas10.4mgL−1(SD±2.1).In2013meanwater
temperaturewas25.6◦C(SD±2.1),meanpHwas7.6(SD±0.4),
meanconductivitywas109S/cm−1(SD±2.6)andmeandissolved
2.3. Movementdistances
CrayfishradiolocationdatawereanalyzedonArcGIS v10.1,
usingHawth’s tools 3.27(Beyer, 2004)and FishTracker(Laffan
and Taylor, 2013) for straight line movement analysis and for
movement analysis accounting for the curvature of the river,
respectively. FishTrackeris open sourceand waswritten using
theESRIarcpysystem.Itcancalculateleastcostpathsbasedona
costsurfacemapandwasoriginallydevelopedtostudyfish
move-mentsinestuarinesystems(LaffanandTaylor,2013).Inourcase
thecostsurfacemaprestrictedthemovementpathstotheriver
bedarea,notallowingforoverlandmovement.Weextractedthe
distancesbetweentheconsecutivedetectionpointsfromthe
geo-processinglogofFishTracker.Basedontherecordedmovement
anddirectionofmovementforeachindividual,Euclideandistances
wereobtainedusingHawth’stools.Thesedistanceswereplotted
ona circulardiagram andanalyzed forrandomnessusingRao’s
spacingtest.Themedian,rangeofvaluesanddistributionofthe
pooleddistancesmovedbyallcrayfishofeachspecieswas
com-paredusingtheMediantest,theMosestestofextremereaction
andaKolmogorov–Smirnovtest,respectively.
Meandailymovementofeachindividualwasobtainedby
divid-ingthesumoftheobserveddisplacementdistances(correctedfor
thecurvatureoftheriverusingFishTracker)bythenumberof
track-ingdays.
AMANOVAwasapplied,wheretheindependentvariableswere
speciesandyearandthedependentvariablesweremeandaily
dis-tancetraveled,maximumobservedEuclideandistancefromthe
pointofreleaseandthepercentageofobservationsunder
vegeta-tioncoverforeachindividual.ALOG10transformationwasapplied
tothevariables:meandailydistanceandmaximumobserved
dis-tancefromthepointofreleaseandtheassumptionsofMANOVA
werestatisticallytestedandwerenotviolated.AftertheMANOVA,
anANOVAwasappliedtoeachdependentvariable.Thisallowedus
toidentifywhichdependentvariableswereaffectedbythetested
factors.
Statisticalanalysesonnon-circulardatawereperformedusing
IBMSPSSv.20.CirculardatawereanalyzedusingOriana4.02.
2.3.1. Upstreamvs.downstreammovements
WeusedaChi-Squaredtestonacontingencytabletoanalyzeif
theproportionofupstreamordownstreammovementswas
inde-pendentofthespecies.Toassesstheconsistencyofthemovement
direction(Idir)andofthedistancesmoved(Idist)byeachcrayfish,
twoindicesweredeveloped:
Idir=|ndownstream−n upstream|
Largest n
wherendownstreamorupstreamarethetotalnumberof
move-mentsineachdirection,respectively
Idist=
downstream distances−upstream distancesLargest
where the distances are the Euclidian distances between two
consecutive detection locations (downstream and upstream,
respectively).
2.3.2. Spaceuseandmesohabitatpreferences
Tobetterevaluatespace useby thesespecies, we produced
kerneldensitymapsforeachindividual,showingthesizeofthe
areaswithmoreintensepatternofuseandalsoiftherewasa
sin-gleareaormultipleareasofintenseuse.Thekerneldensitymaps
wereproducedbyFishTrackerusingtheaccumulatedtransitraster
withintheriverasthelocations,weightedbytheirtransittimes
(LaffanandTaylor,2013).Thissoftwareexcludedthepossibilityof
Table1
MANOVAresults,usingspeciesandyearasindependentvariablesandthemean dailydistancetraveled,themaximumobserveddistancefromthepointofrelease andthepercentageofobservationsundervegetationcoverasdependentvariables.
Effect Pillai’strace F Hypothesisdf Errordf Sig.
Intercept 0.976 173.350 3 13 0.000
Species 0.594 6.338 3 13 0.007
Year 0.504 4.409 3 13 0.024
Species*year 0.305 1.904 3 13 0.179
overland movements between two detection points, always consideringtheshortestpathwithintheriverbed.Kerneldensity surfacesweremaskedbytheriverbed.The50thand90thpercentile surfacesofthekerneldensitysurfaceexcludingzerovalueswere calculatedbythesamesoftwareandthecorrespondingareaswere extracted.Toassesshabitatpreferencesofeachindividual cray-fish,weappliedtwoindicesfrequentlyusedforfoodpreference butpreviouslyusedforhabitatpreferences(e.g.Loughmanetal.,
2013).TheseweretheIvlev’sElectivityIndex(Ivlev,1961),andthe
StandardizedForageRatio(Chesson,1983)whichismorerobust.
Botharepresentedbelow.
Ivlev’selectivityindex,Ei(Ivlev,1961)adaptedforhabitattypes
(i):
Ei= rri−Pi
i+Pi
whereriistheproportionofobservationsoftheindividualcrayfish
inahabitattype(i)andPiistherelativeabundanceofthathabitat
inthestudyarea.EiisscaledsothatEi=−1correspondstototal
avoidanceofthehabitattype(i),Ei=0representsnon-selectiveuse
ofhabitattype(i),andEi=1showsexclusiveuseofhabitattype(i).
StandardizedForageRatio(Chesson,1983)adaptedforhabitat
types(i):
Si=
nri/Pin=1(rn/Pn)
whereriandPiaredefinedasabove,andnisthenumberofhabitat
typesinthestudyarea.Thestandardizedforageratioasoriginally
presentedtakesvaluesbetween0and1,withSi=0representing
avoidanceofhabitattype(i)andSi=1exclusiveuseofhabitattype
(i).
3. Results
3.1. Movementdistances
PooledmovementdataofP.clarkiiand P.leniusculusdiffered
significantly in relation to median, range of values and
distri-butions (n=751and p<0.001 for all tests: median test, Moses
test of extreme reaction and Kolmogorov–Smirnov test). The
meanmovement(forbothyears)was8.8mday−1(95%confidence
interval:2.575–15.025) forP.clarkii and17.5mday−1 (95%C.I.:
8.554–26.446)forP.leniusculus(Fig.3).However,crayfish
behav-iorrangedfromalmostcompleteimmobility,sometimesforseveral
days,tolargemovements,inahalfdayperiod,reachingamaximum
of255mforP.clarkii(Fig.4)and461mforP.leniusculus(Fig.5),
calculatedwithFishTracker.Forthemajorityofthetimetherewas
nocrayfishmovementbetweenconsecutivesurveysandthis
pat-ternwasthesameforbothspecies(Fig.3d).Usingvaluesfromboth
years,P.clarkiiandP.leniusculusdidnotmoveon67.6%and57.95%
ofthehalfdayperiods,respectively.
A MANOVA (Table 1) showed that thefactors ‘species’ and
‘period’ significantly affected crayfish movement and location
metrics.Thetestalsoshowedthattherewasnointeractionbetween
Fig.3. Averagevaluesofthecollecteddataregardingspaceuseandmovement.Meanvaluesarepresentedforeachyearandspecies.Meandistanceattheendisthemean distanceofthelastdetectionofeachcrayfish.Errorbarsarethestandarderrors.7P.clarkiiand12P.leniusculusweretrackedtwiceperdayduringameanperiodof21days. Dataobtainedfromatotalof741radio-locationpoints.
thedependentvariables (Table2), foundsignificantdifferences
betweenspecies(p=0.001),regardingthepercentageof
observa-tionsundervegetationcover.Themaximumobserveddistances
fromthepointofreleaseweredifferentin2010and2013(p<0.05).
Actually,contraryto2010,in2013P.clarkiialwaysremainedinthe
vicinityofthereleasepoint.Thisresultedinasignificantinteraction
(p<0.05)betweenspeciesandyearinwhatconcernsthemaximum
observeddistancefromthepointofrelease.
Asexpected,crayfishmovementsweremainlyorientedonan
upstream/downstreamaxis(Fig.3f),withminormovements
per-pendiculartotheriver.Consequently,Rao’sspacingtestshowed
thatmovementswerenotrandomlydistributedinalldirections
foreitherofthetwospecies(Fig.6).
3.2. Upstreamvs.downstreammovements
The proportion of upstream or downstream movements
was independent of the species (Chi-squared test, X2=0.195,
d.f.=1, p=0.659). In fact, both species have a proportion of
upstream/downstreammovements not differing from1/1
(Chi-squaredtest;P.clarkii,X2=2.042,d.f.=1,p=0.153;P.leniusculus,
X2=1.843,d.f.=1,p=0.175).Thevaluesobtainedfromthe
move-mentconsistencyindices(IdirandIdist,Figs.4and5)showedalarge
interindividualvariation,withsomevaluescloseto1indicatinga
highconsistencyandothervaluesclosetozero,indicatinglackof
consistency.MeanIdirwas0.4and0.49forP.clarkiiandP.
leniuscu-lus,respectivelyandmeanIdistwas0.58and0.65alsoforP.clarkii
andP.leniusculus,respectively.
3.3. Spaceuseandmesohabitatpreferences
Considering datafromboth years,P.clarkii individuals were
locatedata meandepthof36.2cm(min:17.6;max: 60.7)and
P.leniusculusatameandepthof45.2cm(min:22.8;max:87.3)
(Fig.3f).Figs.7and8showthatcrayfishoccupiedasmallportionof
theavailablespaceforaperiodoftimeandthenmovedtoanother
smallarea.ThisbehaviorwasmorepronouncedforP.leniusculus
thanforP.clarkii.Theaverage50thpercentileareasofthekernel
densitiesobtainedwithFishtrackerwere1232m2(min:153;max:
3252)and1519m2(min:275;max:3298)forP.clarkiiandP.
lenius-culus,respectively.Theaveragesizeofthe90thpercentilekernel
densityareaswere2087m2(min:282;max:5733)and2719m2
(min:488;max:5949)forP.clarkiiandP.leniusculus,respectively.
Toassesshabitatpreferences,weappliedtheIvlev’sElectivity
IndexandtheStandardizedForageRatio.Bothindicespresented
similarresults(Fig.9)withP.clarkiishowingapreferenceforpool
areaswithriparianvegetationcoverwhileP.leniusculuspreferred
riffleandpoolareaswithriparianvegetationcover.Bothspecies
clearlyavoidedrunareas,withorwithoutvegetationcoverand
alsoriffleareaswithoutcover.
4. Discussion
Thereweredifferencesamongthetwospeciesandalsoamong
the2010and2013radio-trackingperiodsregardingthe
descrip-torsofmovementandspaceuse.Thedifferencesbetweenperiods
Fig.4.ProcambarusclarkiimovementsthroughoutthetrackingperiodobtainedusingHawth’stools.Dotsrepresentthedetectedpositionsandsequentialpositionsare representedbylinesdrawnusingHawth’sTools.Eachcrayfishisidentifiedonthetopofthefigurebythefrequencyofitstransmitter.Idir–consistencyofthemovement
directionandIdistconsistencyofthedistancesmoved;0–lackofconsistency,1–totallyconsistent.
conditions,suchasphotoperiod,rainfall,flow,temperatureor
oxy-genavailabilitywhichcanaffectcrayfishmovementandactivity
(Flint,1977;Abrahamsson,1983;Gutierrez-Yurrita andMontes, 1998;Robinsonetal.,2000;Vicky,2000;Bubbetal.,2004).Another
non-exclusiveexplanationwouldbethatcrayfish–alladultsof
approximatelythesamesize–couldpossiblybeatdifferentlife
cyclestages.Ithasbeendescribedthatundercertaincircumstances
thismayalsoaffectdispersionpatterns(GherardiandBarbaresi,
2000;Light,2003).P.clarkiimainrecruitmentperiodinPortugal
isusuallyin September/October(Anastácioand Marques,1995;
Anastácioetal.,2009)andmatingisduringMay–July.Althoughno
differencesinreproductiveformwereperceptibleamong2010and
2013individuals,the2013trackingperiodwasjustaftertheusual
matingperiod.Inwetlandsareas,matingisfrequentlyfollowedby
burrowing,especiallyoffemales.
P.leniusculusmovedmorethanP.clarkii(17.5and8.8mday−1,
respectively)andthesevaluesarewithintherangepresentedinthe
literatureonthesespecies(Table3).Usingasimplifiedapproach,
i.e.assumingcontinuousmovementinonedirectionwithout
bar-riersorwithoutperiodsofinactivity,thiswouldbeconvertedto
3.2kmyear−1forP.clarkiiand6.4kmyear−1forP.leniusculus.These
arehigherthantheaveragevaluesfortheprogressionofthe
inva-sionfrontinthearea(Bernardoetal.,2011).Possibleexplanations
forthesehighervaluesaretheabsenceofaperfectdirectionality
inthemovementandalsothefactthatthecurrentstudywas
per-formedduringthesummerandautumnwhentemperatureswere
warmandcrayfish aremoreactive(Araujoand Romaire,1989;
Bubbetal.,2002).
Afewauthorsrefertotheoccurrenceofafrightresponsein
thefirstdaysafterreleaseofradiotaggedcrayfish(Robinsonetal.,
2000)orimmediatelyafterintroductionintoanewarea(Fürst,
1977).Justlikeseveralotherauthors (Vicky,2000; Bubb etal.,
2002;Buricetal.,2009),wefoundnoclearevidencesupportingthis
typeofbehavior.Notwithstanding,wefoundalarge
interindivid-ualvariabilityinmovementbehaviorforbothspecies.Thisseems
tobeacommoncharacteristicforseveralcrayfishspecies(Flint,
1977;Robinsonetal.,2000;ByronandWilson,2001;Bubbetal., 2002,2006),whichmayindicatedifferent“personalities”regarding
thepropensityformovementanddispersion,afactorwhichcould
beresearchedinfuturestudies.Additionally,somestudieshave
mentioned thepossibility of coexistence of two spatial
Fig.5. PacifastacusleniusculusmovementsthroughoutthetrackingperiodobtainedusingHawth’stools.Dotsrepresentthedetectedpositionsandsequentialpositionsare representedbylinesdrawnusingHawth’sTools.Eachcrayfishisidentifiedonthetopofthefigurebythefrequencyofitstransmitter.Idir–consistencyofthemovement
directionandIdistconsistencyofthedistancesmoved;0–lackofconsistency,1–totallyconsistent.
populations(Gherardietal.,2000a,b,2002;GherardiandBarbaresi,
2000;Barbaresietal.,2004).Ahighvariabilityinmovement
strate-gies, when associated withsmallsample sizesof radio tagging
studies,caneventuallyaccountforsomeinter-studyvariationin
movementresults.
Large-scale animal movement behavior may be advective
(migratory), confined (home range) or diffusive (nomadic)
(Benhamou,2014)andthelatterseemstofittheobservedcrayfish
movement.Thepatternofmovementofbothspeciesofteninvolved
periodsofimmobilityforseveraldays,interruptedbylarge
move-mentsand intermittenceis commonin animal motion(Harnos
etal.,2000;KramerandMcLaughlin,2001).Fractalintermittence
involvingstops,strongre-orientationsandbehavioral
character-isticinterruptionsmayoriginateastochasticorganizationofthe
search(forexampleforresources)iftheanimalhasalow
percep-tionofthesurroundingconditions(Bartumeus,2007).Thismay
bethecasewithcrayfishmovingonthisriverbed.Bouldersand
largestonesareanimportantcomponentofthesubstratewhich
stronglyreducesthevisualorientationcapabilitiesofthecrayfish
movingontheriverbottom.Moreover,duetowaterflow,the
per-ceptionofolfactoryclues maybereduced sincethesecluesare
mostlyobtainedfromupstreamsources.
Bothspeciesseemedtouseapatchandthenmovetoanother,
andthispatternwasmorepronouncedinP.leniusculus.A
conse-quenceofthisbehavioristhatitmakesitinadequatetoquantify
truehomeranges.Infact,randomwanderingisfrequentinreptant
decapods,withsomestayingwithinahomerangeareawithno
Table2
ResultsoffactorialANOVAs,usingspeciesandyearasindependentvariables.
Source Dependentvariable TypeIIIsumofsquares df Meansquare F Sig.
Correctedmodel LOG10(MDD) 1.159a 3 .386 2.252 .124
LOG10(MOD) 2.617b 3 .872 3.574 .039 %UVC 7064.941c 3 2354.980 5.354 .010 Intercept LOG10(MDD) 14.359 1 14.359 83.670 .000 LOG10(MOD) 59.280 1 59.280 242.846 .000 %UVC 68,074.094 1 68,074.094 154.755 .000 Species LOG10(MDD) .590 1 .590 3.438 .083 LOG10(MOD) .658 1 .658 2.694 .122 %UVC 6798.449 1 6798.449 15.455 .001 Year LOG10(MDD) .196 1 .196 1.144 .302 LOG10(MOD) 1.270 1 1.270 5.201 .038 %UVC 204.035 1 204.035 .464 .506
Species*year LOG10(MDD) .689 1 .689 4.017 .063
LOG10(MOD) 1.392 1 1.392 5.703 .031 %UVC 14.414 1 14.414 .033 .859 Error LOG10(MDD) 2.574 15 .172 LOG10(MOD) 3.662 15 .244 %UVC 6598.237 15 439.882 Total LOG10(MDD) 21.732 19 LOG10(MOD) 79.531 19 %UVC 81,178.060 19
Correctedtotal LOG10(MDD) 3.733 18
LOG10(MOD) 6.279 18
%UVC 13,663.178 18
LOG10(MDD),meandailydistancetraveled;LOG10(MOD),maximumobserveddistancefromthepointofrelease;%UVC,percentageofobservationsundervegetationcover. aRsquared=.311(adjustedRsquared=.173).
b Rsquared=.417(adjustedRsquared=.300). c Rsquared=.517(adjustedRsquared=.420).
(Vannini and Cannicci, 1995). Indeed, Robinson et al. (2000)
referredtothisasephemeralhomerangesandoneconsequence
ofthiswanderingbehavioristhatthelongeracrayfishisfollowed
byradio-tracking,thelargerthe“homerange”recorded(Hazlett
etal.,1974).
LévyWalk isa form ofSimple RandomWalk inwhich turn
andorientationdistributionsareuniformlyrandom,withaheavy
tailedsteplengthdistribution(Benhamou,2014).Lévyprocesses
ofmovementcanbedescribedbyrandomwalkmodelsandamong
thelatterthereareLévyflightandLévywalkmodels.Withlarge
timescalesincomparisontothedurationofmovement,a Lévy
flightapproachismoreadequate.However,inthepresentstudy,
thedurationofthemovementsisrelevantandthereforeLévywalk
shouldprovideasuperiorapproximationwhenmodelingcrayfish
movement.As thesetwo species are currentlyexpanding their
distributionin thearea(Bernardoetal.,2011),ourresultsoffer
valuableinformationformodelingandconsequentlyformanaging
theirspread.
Thedeveloped indices (Idir and Idist)showedlarge
interindi-vidualvariationsintheconsistencyofthedirectionofmovement
but no species specific tendencies were noted. Most of the
half-day movements detected in both species are on an
upstream/downstreamaxisand this islikely due tothealmost
linear structure of the river channel. In fact, lateral
move-ment of the crayfish is limited by the narrow river channel.
The low flow during the periods of theyear when field work
tookplace maybe one of the reasons why theproportions of
upstream/downstreammovementsdidnotdifferfrom1/1.Similar
proportionsofupstream/downstreammovementswerealsofound
forothercrayfishspecies(Robinsonetal.,2000;Bubbetal.,2002;
Kadlecováetal.,2012)aswellasforP.clarkii(Kerbyetal.,2005)
butresultsaremixedforP.leniusculus,withsomeauthorsfinding
somedirectionalityinthemovementalongtheriver(Holdichetal.,
1995;GuanandWiles,1997;Buˇriˇc,2009).
The comparison of the two habitat preference indices
con-firmsthenotionthatalthoughIvlev’sElectivityIndex(Ivlev,1961)
Table3
MovementspeedofP.clarkiiandP.lenisculuspresentedintheliterature.
Species Speed(mday−1) References
P.clarkii 1.1–4.6 Gherardietal.(2000a)
P.clarkii Maximumof4000(inricefieldhabitats) GherardiandBarbaresi(2000)
P.clarkii 0.6–1.5 Gherardietal.(2000b)
P.clarkii 1–11(temporarystream) Gherardietal.(2002)
P.clarkii 2.5–38 Aquilonietal.(2005)
P.leniusculus 13.5upstream
15downstream
Bubbetal.(2004)
P.leniusculus 5(approximatemedian) Bubbetal.(2006b)
P.leniusculus Maximumof600(Introductioninanewarea) Fürst(1977)
P.leniusculus 3.29(downstreamcolonizationrate) PeayandRogers(1998)
P.leniusculus 4.1 Holdich(1991)
P.leniusculus 7.7(downstreamcolonizationrate) 4.6(upstreamcolonizationrate)
Fig.6. Circularplotofallthedataobtainedduring2010and2013regardingthe directionsandtherespectivedistancesmoved.Topfigure–P.clarkii.Bottomfigure –P.leniusculus.Alogarithmicscaleof0–1000misused.TheresultsoftheRao’s spacingtestforrandomnessofdirectionsarepresented(Ustatisticandpvalue).
is widely used, the Standardized Forage Ratio is more robust
(Chesson,1983)andprovidesaclearerpictureofthehabitat
prefer-ences.ThefindingthatP.clarkiipreferspoolareaswithvegetation
coverisinaccordancewithpreviouswork(Aquilonietal.,2005;
Banhaand Anastácio,2011).Actually,P.clarkiiis mostlya
low-landaquaticspeciesandneedstherighttypeofsedimenttobuild
burrows(CorreiaandFerreira,1995),whileP.leniusculusishighly
adaptedtolivinginmountainrivers,asobservedintheIberian
Peninsula(Rallo and García-Arberas,2002).In ourstudy inthe
riverMac¸ãs,P.leniusculusshoweda strongerpreference for
rif-flethanforpoolareas,bothwithriparianvegetationcover.These
resultsaresomewhatdifferentfromresultsobtainedinlakeand
reservoirareaswithinthenativedistribution,inwhichtheadults
Fig.7.KerneldensityplotsforProcambarusclarkii.Theredcolorindicatestheareas withahigherintensityofuseforeachindividual.Eachcrayfishisidentifiedby thefrequencyofitstransmitter.M–male;F–female.(Forinterpretationofthe referencestocolorinthistext,thereaderisreferredtothewebversionofthe article.)
Fig.8.KerneldensityplotsforPacifastacusleniusculus.Theredcolorindicatesthe areaswithahigherintensityofuseforeachindividual.Eachcrayfishisidentified bythefrequencyofitstransmitter.M–male;F–female.(Forinterpretationof thereferencestocolorinthistext,thereaderisreferredtothewebversionofthe article.)
ofthis speciespreferdeep,sandyand lessvegetatedareas (e.g.
AbrahamssonandGoldman,1970;LewisandHorton,1997).
Bothspeciesavoidedrunareas,withorwithoutvegetationcover
andalsoriffleareaswithoutcover.Spatialdisplacement
mecha-nismsduetooneofthespecieshavinganadvantageinaggressive
encounters,e.g.whilecompetingfor shelter,do notseemtobe
Fig.9.HabitatpreferencesofP.clarkiiandP.leniusculus.Twodifferentindicesarepresented.IvlevElectivityindex(E)isscaledsothatE=−1correspondstototalavoidance ofthehabitattype,E=0representsnon-selectiveuseofthehabitattype,andE=1showsexclusiveuseofthathabitattype.TheStandardizedForageRatio(S)takesvalues between0and1,withS=0representingavoidanceandS=1representingexclusiveuseofthattypeofhabitat.
andP.leniusculus(MuellerandBodensteiner,2009).Coexistenceat
asmallscalewasinfactobservedinthisstudy,withnon-tagged
crayfishofbothspeciesoftenbeingvisuallydetectedinthesame
area.
Itwaspossibletoidentifyafewlimitationsinourapproach.
Ourdatado notallowforananalysisof theannualpatternsof
variationin themovement and spaceuse. Since thestudywas
conductedintworestrictedperiods,withdifferentindividualsin
eachperiod,therewasalsonopossibilityofassessingtheeffects
ofenvironmentalvariables (e.g.temperature). Thevaluesofthe
environmentalvariableswereactuallyquiteconservative
through-outthestudy.We considerthat ourresultsreflect a maximum
dispersionofthesespeciesintheareasincethestudywas
per-formedduringtheperiodsoflargestcrayfishactivity.Duetothe
largeeffortinvolvedinradio-trackingstudies,wecouldnotmakea
directcomparisonofasituationwithandwithoutco-occurrenceof
crayfishspecies.Inspiteofthis,inotherspeciesofcrayfishsuchas
Austropotamobiustorrentium,thespreadisdependentonthe
occur-renceofA.astacus(Kadlecováetal.,2012).Fromourresultsitisclear
thatneitherofthespeciesstopsitsactivityduetothepresenceof
thecompetingspecies.
Inaddition,wewereunabletoclearlydistinguishnightandday
movementssincealltheobservationsweremadeduringdaytime,
accordingtothe12-hintervalthatwasused.Althoughcrayfishare
usuallyhighlynocturnal,inpreviousworktheproportionof
day-timemovementswasshowntobesignificantlygreaterinsummer
monthsthaninautumnmonths(Johnsonetal.,2014).
P.clarkiiiscurrentlyestablishedthroughoutalmostallofthe
IberianPeninsula(Souty-Grossetetal.,2006)butisstill
spread-ingtowardsomeheadwaterstreams.Additionally,itisspreading
strongly in other European territories(e.g. Italy; (Scalici et al.,
2010))andtherearestillwideareasenvironmentallysuitablefor
invasionworldwide(Capinhaetal.,2011).Likewise,P.leniusculusis
spreadingovertheIberianPeninsula,withwideareasavailablefor
invasioninthisterritoryandalsoworldwide(Capinhaetal.,2011,
2012).Onamacroscale,thesetwospecieshaverelativelydifferent
environmentalpreferencesbuttheirdistributionsclearlyoverlap
insomeareas,suchasthestudiedriverstretch.Ourworkprovided
newandvaluabledataformodelingthedispersionofthesetwo
speciesinacontextofcoexistence.
Acknowledgements
Wethanktheanonymousreviewerswhogavevaluable
con-tributions for improving this paper. This study was partially
financed by FEDER funds through the “Programa Operacional
de Factores de Competitividade – COMPETE” and by national
funds through “FCT – Fundac¸ão para a Ciência e Tecnologia”
within the scope of the project DID (Dispersal of Invasive
Decapoda)(PTDC/BIA-BEC/105182/2008).InstitutodaConservac¸ão
da Natureza e das Florestas also provided financial support.
FilipeBanhaholdsaPhDgrantfromFCT(SFRH/BD/81378/2011)
andCésarCapinhaacknowledgesfundingsupportfromFCT(grants
SFRH/BD/41129/2007andSFRH/BPD/84422/2012).
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