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Ecology and Evolution. 2018;1–13.
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1
www.ecolevol.org
Received:17July2017
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Revised:9November2017
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Accepted:20November2017
DOI:10.1002/ece3.3739
ORIGINAL RESEARCH
An anthropogenic habitat within a suboptimal colonized
ecosystem provides improved conditions for a range- shifting
species
Zachary J. Cannizzo1 | Sara R. Dixon1 | Blaine D. Griffen2
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,
providedtheoriginalworkisproperlycited.
©2018TheAuthors.Ecology and EvolutionpublishedbyJohnWiley&SonsLtd.
1MarineScienceProgram,SchooloftheEarth,
Ocean,andEnvironment,UniversityofSouth
Carolina,Columbia,SC,USA
2DepartmentofBiology,BrighamYoung
University,Provo,UT,USA
Correspondence
ZacharyJ.Cannizzo,MarineScienceProgram,
SchooloftheEarth,Ocean,andEnvironment,
UniversityofSouthCarolina,Columbia,SC,
USA.
Email:cannizzz@email.sc.edu
Funding information
DivisionofOceanSciences,Grant/Award
Number:OCE-1129166
Abstract
Manyspeciesareshifting their ranges in response to the changing climate. In cases
wheresuchshiftsleadtothecolonizationofanewecosystem,itiscriticaltoestablish
howtheshiftingspeciesitselfisimpactedbynovelenvironmentalandbiologicalinter-
actions.Anthropogenichabitatsthatareanalogoustothehistorichabitatofashifting
speciesmay play acrucial role inthe ability ofthat species toexpand or persistin
suboptimalcolonizedecosystems.Wetestediftheanthropogenichabitatofdocks,a
likelymangroveanalog,providesimprovedconditionsfortherange-shiftingmangrove
treecrabAratus pisoniiwithinthecolonizedsuboptimalsaltmarshecosystem.Totest
ifdocksprovidedanimprovedhabitat,wecomparedtheimpactofthesaltmarshand
dockhabitatsonecologicalandlifehistorytraitsthatinfluencetheabilityofthisspe-
ciestopersistandexpandintothesaltmarshandcomparedthesebacktobaselinesin
thehistoricmangroveecosystem.Specifically,weexaminedbehavior,physiology,for-
aging,andthethermalconditionsof A. pisonii in each habitat. We found that docks
provideamorefavorablethermalandforaginghabitatthanthesurroundingsaltmarsh,
whiletheirabilitytoprovideconditionswhichimprovedbehaviorandphysiologywas
mixed. Our study shows that anthropogenic habitats can act as analogs to historic
ecosystems and enhance the habitat quality for range-shifting species in colonized
suboptimalecosystems.Ifthepatternsthatwedocumentaregeneralacrosssystems,
thenanthropogenichabitatsmayplayanimportantfacilitativeroleintherangeshifts
ofspecieswithcontinuedclimatechange.
KEYWORDS
Aratus pisonii,climatechange,habitatanalog,mangrove,saltmarsh,thermalhabitat
1 | INTRODUCTION
Climatechange is forcingorencouraging manyspeciestoshifttheir
geographic ranges (Canning-Clode, Fowler, Byers, Carlton, & Ruiz,
2011;Sorte,Williams,&Carlton, 2010; Waltheretal., 2002). These
shiftsareoftenassociatedwiththesimultaneousshiftsofecosystem
foundation species (Walther, 2010). However, differential shifting
ratesbetweentheecosystemfoundationspeciesandotherspeciesin
thecommunitycanoccurandmayhavecascadingeffectsoncommu-
nitystructureandecosystemfunction.Whensuchamismatchinshift-
ingratesoccurs,itcanresultinaspeciescolonizinganewecosystem
whichithasneverpreviouslyinhabited (Schweiger,Settle,& Kudrna,
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CANNIZZO et Al.
2008).Colonizationofnewecosystemsasaresultofdifferentshifting
ratesisexpectedtoincreaseas climatechangecontinues(Schweiger
etal.,2008;Walther,2010).
While there has been abundant discussion on the importance
ofcorridors in aiding range-shiftingspecies through increasing hab-
itat connectivity (Hannah, 2001; Heller & Zavaleta, 2009; Krosby,
Tewksbury, Haddad, & Hoekstra, 2010; Williams, Shoo, Isaac,
Hoffmann,&Langham,2008),littleworkhasbeendonetodetermine
how these shifts impact the species themselves.This is particularly
true of rangeshifts which result in the colonization of new ecosys-
tems.Arangeshiftintoanecosystemthataspecieshasnotpreviously
inhabitedexposesthecolonizingspeciestonovelbiologicalandenvi-
ronmentalinteractions. Due to the complexity of these interactions,
predicting how theywill impact both the colonized ecosystem and
thecolonizingspeciescanbedifficult.Theinvasionliteraturecontains
abundantresearchonthe impact ofnovel species oncolonizedeco-
systems(Mooney&Cleland,2001;Salo,Korpimäki,Banks,Nordström,
& Dickman, 2007;Vilá etal., 2011 and references therein).Yet,the
impact of novel habitats on colonizing species is relatively under-
studied(but see Phillips,Brown,& Shine,2010),likelybecausemost
studiesofnovelspecies–ecosysteminteractionsarefoundintheinva-
sionliteraturewheretheinvaderisviewedasunnaturalandtherefore
undesirable.
Amongotherfactors,acolonizingspeciesmayfinditselfinaneco-
systemthat differs greatlyfromitshistoricecosystemin foundation
species,structure,foodsources,andenvironmentalstressors.Barring
preadaptation(Hamilton,Okada,Korves,&Schmitt,2015),thesedif-
ferencesarelikelytoresultinsuboptimalconditionsforthecolonizing
species(Holt,Barfield,& Gomulkiewicz,2005;Keller&Taylor,2008).
Infact,novelbioticandabioticinteractionsresultinthefailureofthe
majority ofintroduced species to establish populations (Williamson,
1996; Zenni & Nuñez, 2013 and references therein). While those
colonizingspeciesthatcanestablishafootholdmaybe abletoadapt
tothese novelinteractionsovertime(Hamilton etal.,2015;Kaweki,
2008;Knope&Scales,2013),earlygenerationswilllikelydisplaysymp-
tomsoflivinginsuboptimalconditionsthatwillaffecttheirfitnessand
potentiallylimittheirfurtherexpansionintothenewecosystem.
Despitethedifficulties faced byacolonizingspecies, pocketsof
habitatwhichreplicatesomeoftheconditionsofitshistoricecosystem
mayexist within the colonized ecosystem. Thesepockets of habitat
canbethoughtofasanalogstothehistoricecosystemofthecoloniz-
ingspecies.Thus,weadopttheterms“habitatanalog”and“analogous
habitat” from the urban and reconciliationecology literature (sensu
Lundholm& Richardson,2010).Habitatanalogs havereceivedsome
attentionasartificialhabitatsfoundinhighlyalteredecosystemsthat
replicateconditionsexperiencedbyspeciesintheirnativeecosystems
(Lundholm&Richardson,2010andreferencestherein).Thesehabitats
rangefromquarries(Tropek&Konvička,2008;Tropeketal.,2010)to
urbanrubble (Grant, 2006) and oftenprovidehabitat and refugefor
speciesthatcouldnototherwisethriveinthesurroundingecosystem
(Chester&Robson,2013;Lundholm& Richardson,2010). Whilethe
termshabitatanalogandanalogoushabitathavepredominantlybeen
usedtorefertothosehabitatsfoundwithinhighlyalteredecosystems,
theterminologyisdirectlyapplicabletopatchesofhabitatwithinnat-
ural,butsuboptimal,colonizedecosystemsthatmorecloselyresemble
the historic ecosystem ofthe colonizer. Whether naturalor anthro-
pogenic,analogoushabitatsand otherrefugesmayprovide benefits
suchasamorefavorablethermalenvironment(Mosedale,Abernethy,
Smart,Wilson, & Maclean,2016;Wilsonetal., 2015), predation ref-
uge (Dumont, Harris, & Gaymer,2011), and higher quality foraging.
Anyofthesebenefitscouldhelpaspeciespersistorexpandmorerap-
idlyintoanotherwisesuboptimalecosystem.Thus,thesehabitatana-
logshavethepotentialtoplayacrucialroleincurrentandfuturerange
shifts.However,theimpactofanalogous habitats and other refuges
onrange-shiftingspecieswithincolonizedecosystemsisrelativelyun-
derstudied(butseeWilsonetal.,2015).
ThemangrovetreecrabAratus pisoniioffersanideal opportunity
toexamine the impacts ofboth a colonizedecosystemand a poten-
tialanalogoushabitatonarange-shiftingspecies.Thisarborealcrabis
historicallyassociatedwithNeotropicalmangroveforestsdominated
bythered mangroveRhizophora mangle(Wilson, 1989).However,its
climate-mediated northward range expansion has recently outpaced
thatofthe mangrove ecosystemresultinginthe colonizationofsalt
marshesin the southeastern UnitedStates (Riley,Johnston,Feller,&
Griffen,2014).Thesaltmarsh,whichisdominatedbythegrassSpartina
alterniflora,differsgreatlyfromthe mangroveforestswhereA. pisonii
hashistoricallybeen found.Themangroveprovidesashadedhabitat
withtallverticalstructureandeasyaccesstotheprimaryfoodsource
ofA. pisonii,R. mangleleaves(Beever,Simberloff,&King,1979;López
&Conde,2013),whichareabsentinthesaltmarsh.Thus,A. pisoniiin
thesalt marshfindthemselves inanecosystemwhich differsgreatly
in structure and foragingopportunities from that to which they are
adapted.As a result,A. pisoniiinthesaltmarshdisplaysmaller body
sizes,smallerclutch sizes, and lower larval quality than conspecifics
in the mangrove(Riley & Griffen, 2017). Thus, it appears that com-
paredtothehistoricmangrove,thesaltmarshisasuboptimalhabitat
for A. pisonii. However,A. pisonii is alsofoundon the anthropogenic
habitatofdockswithinthesaltmarsh.
Analogoushabitatsconferbenefitsonaspeciesbybeinginsome
way similar to its historic ecosystem. Docks may fit this criterion
withinthesaltmarsh astheyprovideA. pisoniiwith ashadedhabitat
and vertical structuremore similar to the historic mangrove as well
aseasyaccesstofoodin theformofabundant foulingcommunities.
Whilemangroveleaves are not available in the dock habitat, animal
material,which isabundantondocks in the formoffoulingcommu-
nities,isahigh-qualityfoodsource(Riley,Vogel,&Griffen,2014)that
ispreferredbyA. pisoniiovermangroveleaves(Erickson, Feller,Paul,
Kwiatkowski,&Lee,2008).Easyaccesstoahigh-qualityfoodsource
couldbe a boon to A. pisonii as the quantity and quality ofdiet play
crucialrolesintheenergeticsandlifehistoryofanindividual(Charron
etal.,2015;Wen,Chen,Ku,&Zhou, 2006).The shadedhabitatpro-
videdbythe dock itself, which is similartothe shade providedbya
mangrovecanopy,maybeanadditionalbenefitasthethermalhabitat
experiencedbyanorganismhasadirectimpactonitsphysiologyand
lifehistory(Huey,1991;Leffler,1972), especiallywhenwarmerthan
optimal(Gillooly,Brown,West, Savage,&Charnov,2001). Thus, the
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CANNIZZO et Al.
structure,food,andshadeprovidedbydocksmayallowthemtopro-
videimprovedhabitat forA. pisonii withinthesuboptimal salt marsh.
The use of anthropogenic structures to provide favorable habitat
forspecies experiencing adverseeffectsof climate changehasbeen
proposed (Shoo etal., 2011) and implemented (Mitchell, Kearney,
Nelson,&Porter,2008)asanaspectofadaptivemanagement(Heller
&Zavaleta,2009). However,these structures havealwaysbeende-
signedtocounteractnegativeimpactsexperiencedbyspeciesineither
theirhistoricorhighlydegradedecosystems.Unliketheuseofshade-
clothshelters(Mitchelletal.,2008)andartificialburrows(Souter,Bull,
&Hutchinson,2004),docksrepresentananthropogenichabitatfound
in a colonized natural ecosystemthat was not intended to improve
habitatconditions.
Weexaminetheimpactofthesaltmarshanddockhabitatsoneco-
logicalandlifehistorytraitsofA. pisoniithatinfluencebothindividual
performanceandtheabilityofthisspeciestopersistandexpandinto
thesaltmarsh.This includes aspects of behaviorrelatedto diet and
energystorage, thermal conditionsexperiencedbyA. pisonii, andan
explorationofdietaryintakeandqualityineachhabitat.Wecompare
individualsfromthecolonizedhabitats(saltmarsh anddock)to each
other and to a baseline of conspecificsfrom the historic mangrove
ecosystem.Wetest the overarchinghypothesisthat, in each aspect,
A. pisoniifoundondockswithin thesaltmarshwillbemoresimilarto
conspecificsinthehistoricmangrovethantothoseinthesurrounding
saltmarsh.
2 | METHODS
2.1 | Study species
Aratus pisonii is a mangrove-associated crab found throughout the
Neotropics(Rathbun,1918;Warner,1967).Thislargelyarborealsem-
iterrestrial crab has an ecology that is closely tied to the mangrove
trees themselves (Beever etal., 1979; Warner, 1967). In fact, while
itwillfeed opportunistically on high-qualityanimalmaterial (Beever
etal.,1979;Ericksonetal.,2008),itsprimaryfoodsourceisfreshman-
grove leaves, specifically from the red mangrove R. mangle (Beever
etal., 1979; López & Conde, 2013). Individuals maintain strong site
fidelitytoindividualtrees,abehaviorlostinthesaltmarsh,fromwhich
theytend to moveonlya short distance(Cannizzo& Griffen, 2016).
Despitethis fidelity, this crab isnot aggressively territorial, it is not
uncommon to see numerous individuals in close proximity, and the
FIGURE1 Mapofthelocationofstudy
sites,northernmostAratus pisonii(Riley,
Johnstonetal.,2014),andnorthernmost
black(Avicennia germinans)andred
(Rhizophora mangle)mangroves(Williams,
Eastmanetal.,2014;Williams,Lundholm
etal.,2014).Themapalsodisplaysapoint
delineatedastheextentofthemangrove-
dominatedecosystem.Whilethetransition
frommangrovetosaltmarshexists
asamosaic-likeecotone,thislocation
representsanareawithroughly50:50
mangrove:saltmarshcoverage(Rodriguez,
Feller,&Cavanaugh,2016;ICFellerpers.
com.).Northofthisline,mangrovescan
stillbefoundbutareprogressivelymore
isolatedandexistasindividualsorsmall
patcheswithinasaltmarsh-dominated
ecosystem
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CANNIZZO et Al.
speciesmaintainsasizeandsex-basedsocialhierarchylargelythrough
ritualisticdisplays(Warner,1970).Further,thisspeciesislargelyter-
restrial,returningtothewateronlytowetitsgillsandreleaselarvae,
andeven exhibitsa characteristic climbingbehavior to avoidaquatic
predatorswhenthetiderises(Warner,1967;Wilson,1989).
2.2 | Site description
We examined A. pisonii in mangrove forests in the vicinity of Fort
Pierce, Florida, while individuals in the salt marsh and dock habi-
tatswerefound in the vicinity of Saint Augustine, Florida (Figure1;
TableS1).ThemangrovesitesarewithinthehistoricrangeofA. pisonii
(Rathbun,1918;Warner,1967), whilesalt marshanddocksitesrep-
resenthabitats within the recently colonized region (Riley,Johnston
etal.,2014).Thesiteschosenwereselectedastheyarerepresentative
oftheirrespectivehabitattype.Studiedsaltmarshsites werealways
atleast0.75kmfromthenearestdock to prevent the possibility of
examiningcrabsthathaveaccesstothedock habitat.Whiletwosalt
marshsitesandone docksiteweresouthof thenorthernmostman-
grove(Figure1),mangroves are scarce in this salt marsh-dominated
ecosystemandtendtoexistonlyinsmallisolatedpocketsofindividu-
als.Further,onlyonesiteofeachhabitatissouthofthenorthernmost
redmangrove, the species to which theecologyofA. pisoniiis most
closelytiedinthemangroveecosystem(Beeveretal.,1979;Warner,
1967).Whileitwasimpossibletoensurethattherewasnomovement
betweenthedockandsaltmarshforcrabsexaminedondocks,crabs
tendtoexhibitlittlemovementfromacentralforagingarea(Cannizzo
&Griffen, 2016). Further, evenifthere is some movement between
thehabitats,thiswouldresultinaconservativetestofourhypotheses
byminimizingobserveddifferences.
2.3 | Behavioral observations
Weobservedthebehaviorofindividualcrabsin situ.Ineachhabitat,
wecollected groups of five adult A. pisonii byhand and determined
thesexandcarapacewidth(tothenearest0.1mm)ofeachindividual.
Thegroupsofcrabsweremadeupofthefirstfiveindividualsthatwe
encountered and could capture and were drawn from all accessible
habitats. We then painted the carapace of each crab an identifying
colorwithnailpolishtoaidinidentificationand visibility.Preliminary
experimentsdeterminedthatpaintingthecarapacesofcrabsdidnot
alter their behavior or thermal properties. Following a short period
of observation to ensure normal behavior, we released the crabs
ontoa single tree within 10mof the collection tree of all individu-
als(mangrove), ontoseparateS. alterniflora stalkswithin10m ofthe
areaofcollection(salt marsh), or onto the same piling (dock) of the
dockwhere all individuals were captured. Releasingcrabsneartheir
capturelocation allowedforobservationwhile alsoensuringas near
anaturaldistributionofcrabsaspossible.Toavoidimmediateretreat
into holes, release in the salt marsh occurred during the rising tide
whenthecrabshadnoaccesstothesediment.
Inallhabitats,A. pisoniiclimbsstructureasthetiderisestoremain
outofthe waterandwill even leave occupiedsheltertodo so (per-
sonalobservation).Thus,weobservedcrabsinthemangroveandsalt
marshhabitats from the time they lost access to the sedimentuntil
the receding tide onceagain allowed access to the sediment (~6hr
depending on site and day). In contrast, in the dock habitat, crabs
generallylack access to the sediment throughout the tidal cycle. To
obtain an observational period similarto that of the other habitats,
wethereforeobservedcrabsondocksfrom3hrbeforeslackhightide
until3hrafterslackhightide.Wewatchedcrabsfromadistanceusing
binocularsto avoidimpacting theirbehaviorand monitoredthe indi-
vidualscontinuouslythroughouttheobservationalperiod.Theobser-
vationallocationwaschosen to maximizevisibility,andthe observer
wasfree to move if increasedvisibility was necessary.Behaviorwas
recordedevery 5min and at every change in behaviorwithin those
5-min intervalsasone offour categories:feeding, sitting,moving,or
not-visible (Table1).Each group offivecrabs was only observed for
behavioronce,andonlyonegroupofcrabswasobservedonanygiven
day.AllobservationsoccurredfromMaythroughAugust.
Weseparated the observations into ebb and flood tidal periods
to examine differences in foragingbehavior as crabs gained or lost
accesstofoodsourcesonthesedimentandwethabitatstructure.To
avoidbiasingthedatawithcrabsthatwerenotvisibleforlongperiods,
wealsoremoveddatafromindividualsthatwerenotvisible formore
than66%ofthetidalperiod.Thiscorrectionresultedin theobserva-
tionof38, 55, and 39 individuals duringflood tide and 41, 54, and
39individuals duringebb tide inthe mangrove,salt marsh,anddock
habitats,respectively.Unlessotherwisestated,theseindividualcrabs
weretreatedasthereplicatesforallassociatedstatisticalanalyses.
To test for the effects of multiple biological and environmental
variablesontheproportionoftimespentfeedingduringfloodorebb
Behavior Description
Feeding Thecrabisobservedactivelymovingitsclawsfromafooditemorsubstratetoits
mouth.
Moving Thecrabisactivelymovingalongasubstrateandnotfeeding.Otherenergy-
expendingnonfeedingactivities,suchasritualaggression,werealsoclassified
undermovingastheyrepresentanexpenditureofenergy.However,these
activitieswererareandshort-lived
Sitting Thecrabisnotactivelymoving,feeding,orparticipatinginanyactivity
Not-
visible
Thecrabisnotvisibletotheobserver
TABLE1 Ethogramdescribingthe
behavioralcategoriesassignedwhile
observingAratus pisonii
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CANNIZZO et Al.
tide,weranageneralizedlinearmixedmodelwithabinomialerrordis-
tribution.We included carapacewidth,sex,habitat,airtemperature,
andtide(ebborflood) asexplanatoryvariables.Wealsoincludedthe
individualcrabIDasarandomfactortoaccountforthemultipleobser-
vationsofindividualcrabs(ebbandfloodtide)andweightedthemodel
bythe total time ofobservation for eachindividual.Additionally,we
exploredtheproportionoftimeA. pisoniispentmovingbyemployinga
similargeneralizedlinearmixedmodelbutwiththeproportionoftime
individualsspentmovingastheresponsevariable.
2.4 | Exposure to thermal microhabitats
To explore the thermal conditions experienced by A. pisonii in each
habitat,we compared the solar exposurethey experienced. We did
thisby recording thepositionof crabs as insunor shade duringthe
behavioralobservationsdescribedabove andcalculatingthe propor-
tionof time they spentinthesun. To confirm theinherentassump-
tionthatindividualsexperiencehighertemperatureswhileinthesun,
weplacedHOBO thermal data loggers underneath a dock, and in a
nearbysaltmarshatthesamesiteattachedtoawoodendowelhigh
enough to remain out of the water. These loggers simultaneously
gatheredtemperaturedataeveryminute fromnoon on8 September
2016tonoon on11September2016.Theloggerdatawerenot col-
lectedcoincident with observations of crabsas it was not intended
to measure the exact temperatures crabs experienced but relative
differences between temperatures in the sun and shade. While we
tookadvantage ofthestructural differences betweenthesehabitats
toobtaindatapertainingtotemperatureexposurewhilecrabsarein
thesun(saltmarshlogger)and shade (dock logger), these measures
donot necessarily represent the thermal conditions experiencedby
allcrabs ineachof the twohabitatsat all times.Rather,as the dock
andmangroveprovide shadedcanopies andthe saltmarshdoesnot,
they represent the difference in the thermal conditions most often
experiencedbythecrabsineachhabitat.
To further examine the thermal habitat experienced by the ob-
servedcrabs,weusedaFLIRinstrumentsC2compactthermal imag-
ingcameratotakeathermal imageofeachvisiblemarkedcrabevery
15min throughout the observational period. The days when crabs
were observed took place over a wider range of air temperatures,
which was measuredon site, in the mangrove and salt marsh habi-
tatsthanondocks.Thus,toavoidtheconfoundingfactorofrelatively
coolerairtemperaturesinthesehabitats,onlythermalpicturestaken
ondayswhichhadanaverageairtemperature>29°Cwereexamined.
Thistemperaturerepresentedthelowerboundofairtemperatureson
days crabswere observed in the dock habitat. Alongwith the elim-
inationofphotographswhere no crabswerevisible, thisresultedin
theanalysisof455,294, and289thermalphotographsfromthe salt
marsh,mangrove,anddockhabitats,respectively.Wethenemployed
theprogramFLIRtoolstoobtainthetemperatureatthecenterofthe
carapaceofeachcrab.
We suspected that the proportion of time crabs spent in both
thewater and thesunwouldimpact their body temperature,sowe
calculated these valuesfor all individuals for which we had thermal
photographs.We compared thesevalues between habitats using an
ANOVA followed by aTukey’s HSD test for multiple comparisons.
Unlessotherwise stated, weimplementedthisstatisticalmethod for
allsubsequentcomparisonsmadebetweenandwithinhabitats.
To explore the factors that influence crab temperature, we av-
eraged the recordedbody temperature of individual crabs over the
courseofanobservationalperiod.Weexpected thatthesolar radia-
tionexperiencedbycrabsoverthecourseofanobservationalperiod
(~6hrdependingonsite andday)wouldimpacttheirbodytempera-
ture.Thus,toexaminetheimpactofsolarexposureoncrabtempera-
ture,weobtainedshort-andlong-wavesolarradiationfromtheNCEP
NorthAmericanRegionalReanalysis(NARR).NARRhasaresolutionof
32kmandcalculatessolarradiationin3-hrintervals.Weobtainedthe
solarradiationatthe gridpointclosesttoeachsiteand averagedthe
sumoftheshort-andlong-wavesolarradiationovertheobservational
period.Thisnumber,inW/m2,wasthenmultiplied bythe numberof
secondsthe crabwas observedtospend in thesunto obtainarela-
tivemeasure ofthe solar energyexperienced overthe observational
period.Thiscalculatedvariablewillhereafterbereferredtoas “solar
exposure”.Wethenranamixedeffectslinearmodelwithhabitat,pro-
portionoftimeinwater,solarexposure,andambientairtemperature
asexplanatoryfactorsfortheaveragedcrabbodytemperatures,which
wereincluded asthe responsevariablein the model. Wealso ran a
similar model with the averagedifference between crab body tem-
perature and the ambient airtemperature as the response variable.
Thismodel allowed us toanalyzethe ability ofcrabsin each habitat
tomaintaina bodytemperaturecoolerthan ambientand explorethe
factorsthatimpactthisability.Inbothmodels,thecontinuousexplan-
atoryvariableswerez-scoredtofacilitatecomparisonoftheirrelative
impactsonthe responsevariable.Duetothesite-fidelitybehaviorof
A. pisonii(Cannizzo& Griffen,2016), somecrabswerephotographed
on multiple days. Thus, to accountfor these multiple observations,
crabIDwasincludedinthemodelsasarandomfactor.Thesemodels
allowedustoexploretheimpact ofthese factorsonboth crabbody
temperaturesandcoolingonthetimescale onwhich theexplanatory
factors wereavailable and meaningful. Finally, we ran linearregres-
sionstodeterminewhethertherewererelationshipsbetweenthepro-
portionof timeindividualsspent in thewaterand sunaswell asthe
timespentinwaterandsolarexposure.
2.5 | Diet and energy storage
Toexamine diet indices and the investment of A. pisonii into energy
storage,we collected individuals from each habitatduring the sum-
mersof 2015 and 2016.Oneachof nine randomly selected daysin
eachhabitat,15individualadultA. pisoniiwerecollectedbyhandand
immediately placed on dry ice. In the mangrove and salt marsh, we
collectedthesecrabsinthreegroupsoffiveatthreedistincttidalpe-
riods: just after losing access to the sediment on the flood tide, at
slackhightide,and just before regaining access to the sediment on
theebbtide.Thisresultedincollectiontimes~3hr apart.Duetothe
constantlackofaccesstosedimentinthedockhabitat,wecollected
crabs3hrbefore,at,and3hrafterslackhightide.Asinthebehavioral
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CANNIZZO et Al.
observations, the first five crabs we encountered were collected at
eachof these tidalperiods.Thiscollection regime resulted inatotal
of135crabsfromeachhabitat(45fromeachtidalperiod)whichwere
kept frozen until dissection. No measured indices differed between
years,andthus,datawerepooledacrossyearsforanalysis.
Based on preliminary observations in the laboratory, the gut
clearancetime ofA. pisonii is ~3hr.Therefore,our collection regime
allowedfortheanalysisofdietwhencrabshadaccesstothesediment
(collectedon the flood tide), when crabs only had access to unsub-
mergedhabitat(collectedatslack hightide),andwhen crabshadac-
cesstorecentlysubmergedhabitat(collectedontheebbtide).Priorto
dissection,wedeterminedthesexandcarapacewidth(tothenearest
0.1mm)ofeachcrab.
We ascertainedthe gut fullness of each crab to obtain a snap-
shot of the quantityof food consumed during each tidal period by
removingthe gut contentsanddrying them at 60–70°C to constant
weight.Westandardizedgutfullnessbydividingthe massofthegut
contentsbythevolumeofthegut(
V=
a
(√2∕12)×Gut width3
,where
aisa correctionfactorof0.92forcrabs[Griffen&Mosblack,2011]).
Wethenemployeda two-wayANOVAtocompare the standardized
gutfullness betweentidal periodswithinand betweenhabitats.Due
to inclement weatherduring one observation day in the dock habi-
tat,crabswerecollectedwithout regardfortidalperiod.Thisleadto
only120crabsfromthedock,40pertidalperiod,beinganalyzed for
gutfullness.Asthiswastheonlydissectionparameterdependenton
timeofcollection (seebelow),onlygutfullnesswasimpactedbythis
reducedsamplesize.
Inadditiontodietquantity,weexploredlong-termdietqualityby
measuring the cardiac stomach ofeach crab to the nearest 0.1mm
andcomparingthe gut-width:carapace-widthratio betweenhabitats.
Incrabs,thisratioisaproxyforlong-termdietqualitywithasmaller
ratiocorresponding toahigherquality dietthatlikelycontainsmore
animalmaterial(Griffen&Mosblack,2011).
Toexaminetheproportionalenergeticinvestmentintoenergystor-
agebyconspecificsineachhabitat,weseparatedanddriedtheprimary
energy storage organ(hepatopancreas) (Parvathy, 1971) and the so-
matictissue of each crab. Tocompareenergetic investment between
habitats,wecalculatedthehepatosomaticindex (HSI)ofeachcrabas
the ratio of the dryweights of the hepatopancreas and the somatic
tissue, which is a common measure ofenergy stores in crustaceans
(Griffen,Vogel,Goulding,&Hartman,2015;Kennish,1997;Riley,Vogel
etal.,2014; Sánchez-Paz,García-Carreño,Hernández-López, Muhlia-
Almazán, & Yepiz-Plascencia, 2007). However, HSI is dependent on
bothsex and reproductivestage (e.g.,afemalewill have a lower HSI
whencarryingeggs;Belgrad,Karan,&Griffen,2017).Thus,wegrouped
crabsas male, gravid female, or nongravid female and comparedthe
HSIofthesegroupsbetweenhabitats.Duetoaproblemintransporta-
tion,thelegsofcrabsfromtwotidalperiodsononedayfromtheman-
grovebecamedetachedandmixed.Thismadeitimpossibletoreliably
obtainaweight for somatic tissue from these 10 crabs resulting in a
reducedsamplesizeof125crabsfromthemangroveanalyzedforHSI.
Asthiswastheonlyparameterthatincorporatedsomaticweight,itdid
notaffectthesamplesizeofanyotheranalysis.
2.6 | Statement of animal rights
Allapplicableinstitutionaland/ornationalguidelinesforthecareand
useofanimalswerefollowed.
3 | RESULTS
3.1 | Demographics
Aratus pisonii in the salt marsh habitat were smaller
(CW±SD=12.97±1.57mm) than conspecifics in the mangrove
(17.95±3.12mm) and dock (17.83±2.09mm) habitats (ANOVA,
F2=314.9, p<.001; Tukey’s HSD, p<.001, FigureS1). However,
individuals found in the dock habitat did not differ in size from
conspecificsinthemangrove(Tukey’sHSD,p=.850,FigureS1).
3.2 | Behavioral observations
For the results presented below, “estim.” refers to the parameter
estimate for the statistical model being reported. The propor-
tion of time A. pisonii spent feeding was lower in the mangrove
(Prop. time±SD=0.152±0.139) than the dock (0.190±0.162;
GLM,estim.=−0.754,z=−3.01,p=.003) and salt marsh habitats
(0.189±0.190; GLM, estim.=0.792, z=3.28, p=.006) but did
notdifferbetweenthe dockandsalt marsh(GLM,estim.=−0.218,
z=−0.94, p=.349). Time spent feeding was not affected by car-
apace width or sex (GLM, estim.=−0.042, z=−0.99, p=.326;
estim.=0.382, z=1.87, p=.062, respectively), but was influ-
enced by a number of environmental factors. Feeding decreased
as air temperature increased (GLM, estim.=−0.135, z=−6.90,
p<.001),butincreasedasthetidefellandforagingonrecentlysub-
mergedstructurebecamepossible(GLM,estim.=1.460,z=43.28,
p<.001).Timespentfeedingalsodifferedwithinhabitatsandwas
contingent on the tidal period (two-way ANOVA, Habitat×Tide,
F2=8.664,p<.001; Tukey’s HSD, p<.05, Figure2). Additionally,
foraging depended on interactions between the tide and habitat.
Afterslacktide,crabsinthesaltmarshexhibiteda1.4-foldgreater
increase in feeding than crabs on docks (GLM, estim.=3.975,
z=3.63,p<.001)and a 5.7-fold greaterincreasethan conspecif-
icsinthemangrove(GLM,estim.=4.655,z=4.76,p<.001),while
theincreaseinfeedingduringthis period (ebb tide) did not differ
between the mangrove and dock habitats (GLM, estim.=−0.755,
z=0.66, p=.507). As with tidal period, temperature impacted
feedingdifferently between habitats. Individualsinthe dock habi-
tatincreasedtheproportion oftimetheyfedastemperaturesrose
(GLM, estim.=0.526, z=8.74, p<.001; FigureS2), while the op-
positewas observedinboth the mangrove(GLM,estim.=−0.525,
z=−8.73p<.001)andsaltmarsh(GLM,estim.=−0.330,z=−2.22
p<.001)drivingtheoverallnegativeimpactoftemperatureontime
spent feeding. Additionally, the interaction between temperature
andhabitatrevealedthatthisreductioninfeedingwith increased
temperature was greater in the mangrove than in the salt marsh
(GLM,estim.=0.195,z=3.24p=.002).
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7
CANNIZZO et Al.
Movementpatternswere similarto those seen infeedingas the
proportionof time A. pisonii spent movingwasnotcontingent upon
individual size or sex (GLM, estim.=−0.021, z=−0.74, p=.458;
estim.=0.148,z = 1.003 p=.316,respectively),butwasimpactedby
environmental factors. However, in contrast to feeding, movement
decreasedduringebbtide(GLM,estim.=−0.206,z=−4.46p<.001)
andincreasedwith air temperature (GLM, estim.=0.0433, z=2.25,
p=.024). Additionally,individuals in the mangrove spent a greater
proportion of time moving (Prop. time±SD=0.116±0.018) than
conspecifics in the salt marsh (0.032±0.037; GLM, estim.=1.698,
z=9.73, p<.001) and dock habitats (0.040±0.040; GLM,
estim.=1.322, z=7.44 p<.001). However, movement did not dif-
ferbetweenthesaltmarshanddockhabitats(GLM,estim.=−0.293,
z=−1.73p=.084).Theinteraction betweenmovement andtidere-
vealedthatindividualsinthedockhabitatincreasedtheproportionof
timetheymovedafterslacktide(ebbtide)asopposedtothedecrease
inmovement inboththe mangrove(GLM,estim.=−3.658, z=2.49,
p=.021) and salt marsh (GLM,estim.=−6.110, z=−3.44, p<.001)
which drovethe overall negative trend of reducedmovement after
slacktide.However,thedecreaseinmovementduringebbtidedidnot
differbetweenthemangroveand saltmarsh(GLM, estim.=−2.433,
z=−1.78,p=.076).
3.3 | Exposure to thermal microhabitats
The thermal conditions experienced by A. pisonii differed greatly
between habitats. Individuals observed in the dock and mangrove
habitats spent a similar amount of time in the shade (Tukey’s HSD,
p=.938,Figure3a) and more than 18-foldless time in thesunthan
conspecifics in the salt marsh (ANOVA, F2=110.5 p<.001; Tukey
HSD, p<.001, Figure3a). This likely resulted in individuals in the
mangrove and dock habitats experiencing a cooler microhabitat, as
temperaturesrecorded duringtheday were asmuchas 10°C cooler
intheshadeof adockthan inthenearbysaltmarsh (Figure3b).We
confirmedthisconclusionthroughtheanalysisofcrabbodytempera-
turesobtainedfromthethermalphotographs.
Habitatplayedanimportantroleindeterminingcrabbodytempera-
ture.Crabsinthesaltmarshhadhigherbodytemperaturesthanthose
found in the dock and mangrovehabitats (LMER, estim.=−1.1272,
t98=−2.473 p=.0151; estim.=−1.8366, t90=−3.63, p<.001,
respectively; Figure4a). These individuals were also less able to
maintaina body temperature coolerthan the ambient than conspe-
cifics in the dock and mangrove habitats (LMER, estim.=−1.2825,
t106=−3.01 p=.0033; estim.=−2.004, t96=−4.21 p<.001, re-
spectively; Figure4b).Additionally, compared to conspecifics in the
mangrove,crabs in the dock habitathad ahigherbodytemperature
(LMER,estim.=−0.7095,t64=−2.427 p=.0181) and werelessable
to maintain a body temperature cooler than the ambient (LMER,
estim.=−0.7180, t68=−2.56 p=.0126). The temperature of crabs
FIGURE2 Theproportionoftimespentfeeding±SEbyAratus
pisoniiinthemangrove,saltmarsh,anddockhabitatsbeforeand
afterslackhightide.Groupsthataresignificantlydifferentare
denotedbydifferentletters
FIGURE3 (a)Boxplotscomparingtheproportionoftimespent
insunbyAratus pisoniibetweenthethreehabitats.Groupsthatare
significantlydifferentaredenotedbydifferentletters.Ineachbox
plot,andinallotherboxplotsrepresentedinthispaper,themedian
isrepresentedbyaheavyline,theboxrepresentstheupperand
lowerquartiles,whilethewhiskersrepresent95%ofthedataand
circlesshowoutliers.(b)Thermalloggerdataofloggersplacedinthe
shadeunderadock(dashedline)andintheopeninthesaltmarsh
(solidline)from8September2016to11September2016
8
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CANNIZZO et Al.
alsoincreasedwithambient airtemperature (LMER,estim.=0.9765,
t99=8.99p<.001)anddecreasedas a crab spent a greater propor-
tion of its time in the water (LMER, estim.=−2.4725, t98=−2.21
p=.0295).However,theamountofsolarexposureacrabexperienced
did not have a significant impact on its body temperature (LMER,
estim.=−0.3378, t99=−1.64 p=.1036). In addition, crabs main-
tained body temperaturesprogressively cooler than ambient as the
ambienttemperatureincreased(LMER,estim.=−0.7839,t105=−7.51
p<.001), as solar exposure increased (LMER, estim.=−0.4262,
t105=−2.23p=.02813), and as crabs spent more time in thewater
(LMER,estim.=−2.6752,t104=−2.47p=.0152).Further,crabsinthe
saltmarsh spentagreaterproportionoftheir timeinthe waterthan
conspecifics in the mangrove (ANOVA, F2=8.813, p<.001; Tukey
HSD, p<.001; FigureS3)and dock habitats (TukeyHSD, p = .0087;
FigureS3)which did not differinthisregard(TukeyHSD, p = .0732;
FigureS3).Thisisofnoteastherewasapositiverelationshipbetween
thetime a crab spent in thewaterand both thetimeitspentin the
sun and its solar exposure (LM, t103=2.198, p = .030; t103=1.996,
p=.048,respectively).
3.4 | Diet and energy storage
The gut fullness of A. pisonii differed dependent on both habitat
(two-way ANOVA, F2=14.75, p<.001, FigureS4) and tidal period
(two-way ANOVA, F2=15.38, p<.001). In particular, the interac-
tionofhabitatandtidalperiod(two-wayANOVA,F4=5.18,p<.001)
suggeststhat gutfullnesswas dependentona combinationofthese
variables.Whenanalyzedbyhabitat,itisclearthatA. pisoniiwereable
tomaintainaconsistentgutfullnessthroughoutthetidalcycleinboth
themangrove(TukeyHSD,p>.50;Figure5)anddockhabitats(Tukey
HSD p>.50; Figure5). However, despite an overall higher gut full-
ness(Tukey HSD, p<.001, FigureS4), crabsin the salt marsh were
unable to maintain a full gut and thus were likely unable to obtain
sufficientfood,duringthetimewhenthe rising tide restricts access
to food found on the sediment or deposited by water on structure
(Tukey HSD, p<.001; Figure5). During other times in the tidal
cycle,however, crabs in the salt marsh maintainedahighergutfull-
nessthan conspecifics in the mangrove and dock habitats (two-way
ANOVA, F4=5.18, p<.001; Tukey HSD, p<.01; Figure5). In addi-
tion to unreliable foraging, A. pisonii in the salt marsh had a higher
FIGURE4 (a)Averagebodytemperature±SEofcrabsin
eachhabitat.Groupsthataresignificantlydifferentaredenoted
bydifferentletters.(b)Differencesbetweenaveragecrabbody
temperatureandambientairtemperature±SEineachhabitat.
Groupsthataresignificantlydifferentaredenotedbydifferentletters
FIGURE5 BoxplotsshowingthegutfullnessofAratus pisoniiby
tidalperiodinthemangrove,saltmarsh,anddockhabitats.Groups
thataresignificantlydifferentaredenotedbydifferentletters
|
9
CANNIZZO et Al.
gut-width:carapace-width ratio, indicating a lower quality long-term
diet,thanconspecificsineitherthehistoricmangroveordockhabitat,
wheredietqualitywashighest(ANOVA,F2=20.52,p<.001;Tukey’s
HSD,p<.05,Figure6).
Proportionalenergetic investment into energy storage (HSI) was
highestinthemangroveforbothmales(ANOVA,F2=23.27,p < .001;
Tukey HSD, p<.001) and gravid females (ANOVA, F2=29.24,
p<.001; Tukey HSD, p<.001, Figure7). Energy storage was also
greateringravidfemalesinthesaltmarshthanondocks(TukeyHSD,
p<.001,Figure7),but did notdiffer between these two habitats in
males (TukeyHSD, p=.065, Figure7). In nongravid females, energy
storagewaslowestinthedockhabitat(ANOVA,F2=36.13,p < .001;
TukeyHSD, p<.001, Figure7) but did notdifferbetween theman-
groveandsaltmarsh(TukeyHSD,p=.060,Figure7).
4 | DISCUSSION
Compared to the historic mangrove, the salt marsh proved to be a
suboptimal habitat for A. pisonii in every measured aspect of this
study.Further,thisstudysuggeststhattheroleofthedockhabitatin
providingimproved conditionsforA. pisonii within thecolonizedsalt
marshecosystemismixed.Yet,whiledocksdonotprovideimproved
conditionsineveryway,theydoappeartoprovideimprovementsfor
anumberofimportantaspectsofthiscrab’secologyandphysiology.
Oneimportant benefitconferredby docks islargerbody size. While
thereisasyetnoreliablewaytoagethesecrabs(Hartnoll,2001;Vogt,
2012),andthusnowaytodeterminetherelativeimpactsofageand
growthrate,alargerbodysizeisoftenbeneficial.ForA. pisonii,larger
size confers benefits through size-specific dominance hierarchies
(Warner, 1970) and increased reproductive output (Riley & Griffen,
2017),whichinturn benefitsthepopulation. Thus,greatersize isan
exampleofanindividualbenefitprovidedbyananalogoushabitatthat
mayhavecascadingbenefitsforarange-shiftingspecies.
Understanding how analogous habitats confer general benefits,
suchaslargersize,requiresanunderstandingofthemechanismsthat
leadtothosebenefits.Thiscanbeexploredthroughtheexamination
oftheprecisewaysinwhich ananalogoushabitatprovidesimproved
conditions.Forexample,thequantityandqualityofanindividual’sdiet
haveadirectimpact onseveralaspects ofitsecologyandlifehistory
includinggrowth(Buck etal.,2003; Griffen,Guy,& Buck,2008), off-
spring quantity and quality (Green, Gardner, Hochmuth,& Linnane,
2014;Millamena&Quinitio,2000),andbioenergetics(Charronetal.,
2015;Riley,Vogeletal., 2014).Thus,an improveddietmayitselfbe
themechanismbehind otherbenefitsincludingincreasedsize.Docks
clearly provide improved diet and foraging conditions to A. pisonii
through more continuous accessto a higher quality diet than else-
whereinthesalt marsh.However,thehighgutfullness displayedby
crabs in the salt marsh when the sediment is accessibleand during
ebb tide suggests that they exhibit compensatory feeding through
increasedconsumption when foodis available.While compensatory
feedingis commonamong individuals facedwith poordiets,it isnot
alwayseffective (Cruz-Rivera & Hay,2000) and may be hindered by
irregularaccesstofoodinthesaltmarsh.Inadditiontoregularaccess
tofood,docksprovideabundantanimalprotein,ahigh-quality food
(Riley,Vogeletal.,2014),intheformofhigh-densityfoulingcommu-
nities.We regularlyobservedA. pisoniifeedingonfoulingorganisms
suggesting that animal material plays an important role in the im-
proveddietqualityofthesecrabs.
FIGURE6 Boxplotscomparingthegut-width:carapace-width
ratiosofAratus pisoniibetweenthemangrove,saltmarsh,anddock
habitats.Groupsthataresignificantlydifferentaredenotedby
differentletters.Alowergut-width:carapace-widthratiosuggestsa
relativelyhigherproportionofanimalmaterialinthelong-termdietof
theindividual
FIGURE7 Boxplotscomparingtheinvestmentinlong-term
energystorage,calculatedashepatosomaticindex,ofmale,gravid
female,andnongravidfemaleAratus pisoniibetweenthethree
habitats.Groupsthataresignificantlydifferentaredenotedby
differentletters
10
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CANNIZZO et Al.
Similarlytodiet,thethermalconditionsexperiencedbyanorganism
greatlyimpactitsphysiologyandlifehistory(Huey,1991;Leffler,1972).
Thus,improvedthermalconditionsareapotentialmechanismthatcould
leadto otherbenefitsincluding largersize(Huey,1991; Leffler,1972).
ForA. pisonii,docksprovideashadedthermalrefugewhichallowscrabs
tomaintainabodytemperaturethatislower,andlowerthanambientto
agreaterextent,thanconspecificselsewhereinthe saltmarsh.Infact,
theextensive use of shaded areasofthe dock and mangrovehabitats
suggeststhatshadedareasarepreferredbyA. pisoniiandtheexcessive
timeconspecificsfrom thesalt marshspend inthe sunis likelyaresult
ofthehabitatstructure,notpreference.Theuseofthermallysheltered
habitatsinsuchareaswherepreferredthermalconditionsarenotreadily
availableisaprimarywayinwhichspeciesmayaddressregionalclimatic
shifts(Williamsetal.,2008).Whilewefocusedontheabilityofdocksto
providecrabsa coolerhabitat duringsummer months,the abilityofan
analogoushabitattoprovidea warmer microhabitat in winter months
couldalsobevitaltoarange-shiftingspecies.
Despite the cooler conditions providedby docks, the thermal dif-
ferences observed between habitats were less than the disparity in
timespentinthesunwouldsuggest. Onepossibilityisthatcrabsinthe
open-structured salt marsh experience greater convective coolingdue
to increased wind exposure(Ortega, Mencia, & Perez-Mellado, 2017).
However, our resultssuggest that the lower than expected body tem-
peratureofcrabsinthesaltmarshismorelikelyaresultofdifferencesin
thermoregulatorybehavior.Crabsinthesaltmarshappeartothermoreg-
ulatebydipping inwatertocoolthemselvesafterextendedtimein the
sun,aconclusionsupportedbythepositiverelationshipbetweentimein
waterand solar exposure. Indeed, a comparison of the z-scoredmodel
estimatessuggests thatthetime crabsspendin thewaterhas thelarg-
estimpact on boththeirbodytemperatureandtheirabilitytomaintain
abodytemperaturecoolerthantheambient air.Additionally,dippingin
watercouldhaveanadditionalcoolingeffectevenafterthecrabemerges
via evaporative cooling(Eshky, Atkinson, & Taylor, 1995), which could
alsobefurtherenhancedbyincreasedwindexposure.Indeed,incombi-
nationwiththeresultthatcrabsspendmoretimeinthewaterwhenex-
periencinggreatersolarexposure,itispossiblethatthiscouldexplainthe
unexpectednegativeeffectofsolarexposureonthedifferencebetween
crabbodytemperatureandtheambientairtemperature.Thus,whileex-
posuretothesunsurelyhasanacutewarmingimpact oncrabs, itssta-
tisticalimpactislikelyoverpoweredbytheimpactofcoolingwithwater.
The change in thermoregulatorybehavior in the salt marsh sug-
gestsanotherwayinwhichanalogoushabitatsmayprovideimproved
conditions in colonized ecosystems:by allowing individuals to avoid
potentiallycostlychangesinbehavior.Whilebehavioralchangesoften
provide the first response to alteredenvironments (Gross, Pasinelli,
&Kune, 2010; Sih,Ferrari,&Harris,2011; Wong& Candolin, 2015),
theycan lead to costly ecological trade-offs. ForA. pisonii, the need
to thermoregulate may require crabsto temporarily abandon forage
orshelter to move to waterwheretheyare likely exposed to higher
predation (Warner, 1967; Wilson, 1989). In fact, previous work sug-
gestedthatpredationon largeindividuals may be lower in the man-
grovethan the saltmarshwhich may contributetothesizedisparity
betweenthetwohabitats(Riley&Griffen,2017).Itispossiblethatthe
riskofpredationforlargeindividualsisalsolowerondocks,particularly
consideringthelowoccurrenceofsmallindividuals(FigureS1),further
contributing to the larger size of individuals found there. However,
while docks mayallow A. pisonii to avoid risky thermoregulatorybe-
havior,crabs found there exhibit foraging behaviorthat differs from
crabsin themangroveand issimilarto conspecificselsewherein the
salt marsh. Crabs in the dock and salt marsh habitats increasetheir
feedingas thetidefallssuggestingtheyfeed heavily on food that is
eitherdeposited on structureor submerged at high tide. This differs
fromconspecificsinthehistoricmangrovewhichfeedoncontinuously
accessiblemangroveleaves.Like dippinginwater to thermoregulate,
following recedingwater to feed may increase the risk ofpredation
byaquatic predators (Warner,1967; Wilson, 1989).Thus, the ability
ofdocks to allow A. pisonii to avoidpotentiallydangerous behavioral
changesismixed.
Foraging behavioris not the only way docks fail to provideim-
provedconditionsforA. pisonii.Inparticular,theproportionofenergy
stored by crabs in the three habitatsdiffered in unexpected ways.
Whilethe investmentintoenergystorage(HSI) waslower inthe salt
marshthan the historic mangrove habitat, it was lower still in crabs
foundon docks.Thisisparticularly perplexing whenconsideringthe
larger size and improved diet of crabs on docks. It is possible that
thedifferencesin diet observedbetweenhabitatsplaya rolein the
ability of A. pisonii to convertconsumed energy into stored energy.
Alternatively, some unknown energeticexpense or trade-off in the
dockhabitat maylead to adecreasein energystorage. Inanyevent,
the energystorage of A. pisonii warrants further studyand suggests
thatcrabson the docks likely have differentpatternsofenergyuse
thanthose in thesurroundingsalt marsh ecosystem.Given the met-
aboliccostsforcrabs ofstoringlipids inthe hepatopancreas(Griffen,
2017),the lower HSI seenincrabsonthe docks could be beneficial
forindividualsandmayreflectimprovedenergeticefficiencyforcrabs
usingthishabitattype.
While docks appear to provide several important benefits to
A. pisonii in the colonized salt marsh ecosystem,their role as an ana-
logtothe mangroveis clearlymixed.Yet,whatdocks dorepresentis
arelativelyunderstudied aspectofrangeshiftecology: theroleofan-
thropogenic habitat analogs in providing improved conditions within
suboptimalcolonizednaturalecosystems.However,anumberofstudies
haveproposedimplementingartificialhabitats,orhabitatmodification,
to minimize the exposure ofvulnerable species to stressful changing
conditionsintheirhistoricecosystems(Shooetal.,2011;Williamsetal.,
2008).Suchproposalshaveincludedinstallingmicrohabitatrefugesand
sprinklers foramphibians (Shoo etal., 2011), artificial breeding struc-
tures(Shooetal.,2011),shadecloths(Mitchelletal.,2008),andgeneral
habitat restoration using artificial structuressuch as burrows (Souter
etal.,2004)andformedconcrete(Webb&Shine,2000).However,the
useofanthropogenichabitatsinnaturalecosystemsthataspecieshas
neverbeforeinhabitedhasgarneredlittlediscussion.
The construction of artificial habitatsin unsuitable ecosystems to
help/encouragerange shifts has received some discussion as a facet
of adaptive management strategies (Hoegh-Guldberg etal., 2008).
Additionally,therehasbeenarobustdiscussionoftheuseofcorridorsto
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11
CANNIZZO et Al.
aidspeciesintheirclimate-inducedrangeshifts(Hannah,2001;Krosby
etal.,2010).Infact,increasingecologicalconnectivitythroughcitiesand
otherunfavorablehabitats to encouragethe movementofspecies be-
tweennaturalareashasbeenidentifiedascriticaltotheabilityofmany
species to persist in the face of changing climatic conditions(Krosby
etal., 2010; Williams, Eastman etal., 2014;Williams, Lundholm etal.,
2014).Suchdiscussionstendtofocusoncreatingorpreservingnatural
corridorsbetweennaturalareas(Hannah,2001;Krosbyetal.,2010).In
contrast, anthropogenichabitat analogs may increase, ratherthan im-
pede,the successand rateof rangeshifts. Whilethere hasbeensome
exploration of green roofs (Williams, Eastman etal., 2014; Williams,
Lundholm etal., 2014 and references therein), gardens (Goddard,
Dougill,&Benton,2010),street-sidevegetation(Swan,Pickett,Szlavecz,
Warren,&Willey,2011),andotheranthropogenic“stepping-stone”ref-
uges(Chester&Robson,2013;Gledhill,James,&Davies,2008;Santoul,
Gaujard,Angélibert,Mastrorillo,&Céréghino,2009)infacilitatingmove-
mentthroughcitiesandotherunfavorablehabitat,thisworkhaslargely
focusedonbiodiversityconservationandmovementbetweenhabitable
areasas opposed to rangeshifts (but see Grant, 2006).Yet,anthropo-
genicstructures which werenotspecificallydesigned as habitat could
increase the permeabilityof the habitat matrix during range shifts by
providingmorefavorablehabitatthanthesurroundingecosystem.Even
ifanthropogenichabitatanalogsdonotincreasetherateofarangeshift,
theirabilitytoprovideimprovedconditionscouldprovevitaltothesuc-
cessofrange-shiftingspeciesincolonizedecosystems.
Asclimate changecontinuesto forceor encouragespecies to colo-
nizenewecosystems,itwillbeincreasinglyimportanttounderstandhow
theseshiftingspeciesareimpactedbyhabitatswithwhichtheyhaveno
ecologicalorevolutionaryexperience.Theroleofanthropogenichabitats
ashabitatanalogsmayplayacrucialroleinthe outcomeofrangeshifts.
Thus,theexistenceofanthropogenichabitatanalogsshouldbeincluded
inanalysesofthevulnerabilityofspeciestoclimatechange(seeWilliams
etal.,2008foraframeworkforsuchananalysis).Ultimately,theindivid-
ualbenefits conferredbydocks suggest thattheylikelyhave a positive
impacton the population of A. pisonii in the saltmarsh.Therefore, this
studysuggeststhatanthropogenichabitatshavethepotentialtoplayan
importantroleinprovidingimprovedconditionstorange-shiftingspecies
experiencing suboptimal conditions in colonizedecosystems. While no
habitatanalogislikelytoameliorateallnegativenovelinteractionsexpe-
riencedbyrange-shifting species, amelioration of evena small number
ofnegativeimpactswilllikelybe beneficialto bothindividuals andpop-
ulations.Ifthepatterns that we document are general across systems,
thenanthropogenichabitatsmayplayanimportantfacilitativeroleinthe
rangeshiftsofspecieswithcontinuedclimatechange.
ACKNOWLEDGMENTS
The authors thank K. Plumb and L. Carpenter for help with dissec-
tionsaswellasD.WetheyforguidanceinusingthedatafromNARR.
Additionally,we thank I. C. Feller foradvice and guidance. We also
thank the Smithsonian Marine Station at Fort Pierce, FL, and the
Guana Tolomato Matanzas National Estuarine Research Reserve of
St.Augustine, FL,foraid andassistanceduring this study.This work
wassupported by NSFgrantno.OCE-1129166.Thisis Smithsonian
MarineStationcontributionnumber1077.
AUTHOR CONTRIBUTIONS
ZJC and BDG conceived and designed the experiments. ZJC con-
ducted field work and behavioral observations. ZJC and SRD col-
laboratedondissections andthermal imageanalyses. ZJCperformed
statisticalanalyses.ZJCwrotethemanuscript.BDGprovidededitorial
adviceandguidancethroughouttheproject.
CONFLICT OF INTEREST
Nonedeclared.
ORCID
Zachary J. Cannizzo http://orcid.org/0000-0002-0814-7555
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How to cite this article:CannizzoZJ,RiverDixonS,Griffen
BD.Ananthropogenichabitatwithinasuboptimalcolonized
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