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Many species are shifting their ranges in response to the changing climate. In cases where such shifts lead to the colonization of a new ecosystem, it is critical to establish how the shifting species itself is impacted by novel environmental and biological interactions. Anthropogenic habitats that are analogous to the historic habitat of a shifting species may play a crucial role in the ability of that species to expand or persist in suboptimal colonized ecosystems. We tested if the anthropogenic habitat of docks, a likely mangrove analog, provides improved conditions for the range-shifting mangrove tree crab Aratus pisonii within the colonized suboptimal salt marsh ecosystem. To test if docks provided an improved habitat, we compared the impact of the salt marsh and dock habitats on ecological and life history traits that influence the ability of this species to persist and expand into the salt marsh and compared these back to baselines in the historic mangrove ecosystem. Specifically, we examined behavior, physiology, foraging, and the thermal conditions of A. pisonii in each habitat. We found that docks provide a more favorable thermal and foraging habitat than the surrounding salt marsh, while their ability to provide conditions which improved behavior and physiology was 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 suboptimal ecosystems. If the patterns that we document are general across systems, then anthropogenic habitats may play an important facilitative role in the range shifts of species with continued climate change.
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Ecology and Evolution. 2018;1–13.    
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 1
www.ecolevol.org
Received:17July2017 
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  Revised:9November2017 
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  Accepted:20November2017
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
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,
providedtheoriginalworkisproperlycited.
©2018TheAuthors.Ecology and EvolutionpublishedbyJohnWiley&SonsLtd.
1MarineScienceProgram,SchooloftheEarth,
Ocean,andEnvironment,UniversityofSouth
Carolina,Columbia,SC,USA
2DepartmentofBiology,BrighamYoung
University,Provo,UT,USA
Correspondence
ZacharyJ.Cannizzo,MarineScienceProgram,
SchooloftheEarth,Ocean,andEnvironment,
UniversityofSouthCarolina,Columbia,SC,
USA.
Email:cannizzz@email.sc.edu
Funding information
DivisionofOceanSciences,Grant/Award
Number:OCE-1129166
Abstract
Manyspeciesareshifting their ranges in response to the changing climate. In cases
wheresuchshiftsleadtothecolonizationofanewecosystem,itiscriticaltoestablish
howtheshiftingspeciesitselfisimpactedbynovelenvironmentalandbiologicalinter-
actions.Anthropogenichabitatsthatareanalogoustothehistorichabitatofashifting
speciesmay play acrucial role inthe ability ofthat species toexpand or persistin
suboptimalcolonizedecosystems.Wetestediftheanthropogenichabitatofdocks,a
likelymangroveanalog,providesimprovedconditionsfortherange-shiftingmangrove
treecrabAratus pisoniiwithinthecolonizedsuboptimalsaltmarshecosystem.Totest
ifdocksprovidedanimprovedhabitat,wecomparedtheimpactofthesaltmarshand
dockhabitatsonecologicalandlifehistorytraitsthatinfluencetheabilityofthisspe-
ciestopersistandexpandintothesaltmarshandcomparedthesebacktobaselinesin
thehistoricmangroveecosystem.Specifically,weexaminedbehavior,physiology,for-
aging,andthethermalconditionsof A. pisonii in each habitat. We found that docks
provideamorefavorablethermalandforaginghabitatthanthesurroundingsaltmarsh,
whiletheirabilitytoprovideconditionswhichimprovedbehaviorandphysiologywas
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
suboptimalecosystems.Ifthepatternsthatwedocumentaregeneralacrosssystems,
thenanthropogenichabitatsmayplayanimportantfacilitativeroleintherangeshifts
ofspecieswithcontinuedclimatechange.
KEYWORDS
Aratus pisonii,climatechange,habitatanalog,mangrove,saltmarsh,thermalhabitat
1 | INTRODUCTION
Climatechange is forcingorencouraging manyspeciestoshifttheir
geographic ranges (Canning-Clode, Fowler, Byers, Carlton, & Ruiz,
2011;Sorte,Williams,&Carlton, 2010; Waltheretal., 2002). These
shiftsareoftenassociatedwiththesimultaneousshiftsofecosystem
foundation species (Walther, 2010). However, differential shifting
ratesbetweentheecosystemfoundationspeciesandotherspeciesin
thecommunitycanoccurandmayhavecascadingeffectsoncommu-
nitystructureandecosystemfunction.Whensuchamismatchinshift-
ingratesoccurs,itcanresultinaspeciescolonizinganewecosystem
whichithasneverpreviouslyinhabited (Schweiger,Settle,& Kudrna,
2 
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   CANNIZZO et Al.
2008).Colonizationofnewecosystemsasaresultofdifferentshifting
ratesisexpectedtoincreaseas climatechangecontinues(Schweiger
etal.,2008;Walther,2010).
While there has been abundant discussion on the importance
ofcorridors in aiding range-shiftingspecies through increasing hab-
itat connectivity (Hannah, 2001; Heller & Zavaleta, 2009; Krosby,
Tewksbury, Haddad, & Hoekstra, 2010; Williams, Shoo, Isaac,
Hoffmann,&Langham,2008),littleworkhasbeendonetodetermine
how these shifts impact the species themselves.This is particularly
true of rangeshifts which result in the colonization of new ecosys-
tems.Arangeshiftintoanecosystemthataspecieshasnotpreviously
inhabitedexposesthecolonizingspeciestonovelbiologicalandenvi-
ronmentalinteractions. Due to the complexity of these interactions,
predicting how theywill impact both the colonized ecosystem and
thecolonizingspeciescanbedifficult.Theinvasionliteraturecontains
abundantresearchonthe impact ofnovel species oncolonizedeco-
systems(Mooney&Cleland,2001;Salo,Korpimäki,Banks,Nordström,
& Dickman, 2007;Vilá etal., 2011 and references therein).Yet,the
impact of novel habitats on colonizing species is relatively under-
studied(but see Phillips,Brown,& Shine,2010),likelybecausemost
studiesofnovelspecies–ecosysteminteractionsarefoundintheinva-
sionliteraturewheretheinvaderisviewedasunnaturalandtherefore
undesirable.
Amongotherfactors,acolonizingspeciesmayfinditselfinaneco-
systemthat differs greatlyfromitshistoricecosystemin foundation
species,structure,foodsources,andenvironmentalstressors.Barring
preadaptation(Hamilton,Okada,Korves,&Schmitt,2015),thesedif-
ferencesarelikelytoresultinsuboptimalconditionsforthecolonizing
species(Holt,Barfield,& Gomulkiewicz,2005;Keller&Taylor,2008).
Infact,novelbioticandabioticinteractionsresultinthefailureofthe
majority ofintroduced species to establish populations (Williamson,
1996; Zenni & Nuñez, 2013 and references therein). While those
colonizingspeciesthatcanestablishafootholdmaybe abletoadapt
tothese novelinteractionsovertime(Hamilton etal.,2015;Kaweki,
2008;Knope&Scales,2013),earlygenerationswilllikelydisplaysymp-
tomsoflivinginsuboptimalconditionsthatwillaffecttheirfitnessand
potentiallylimittheirfurtherexpansionintothenewecosystem.
Despitethedifficulties faced byacolonizingspecies, pocketsof
habitatwhichreplicatesomeoftheconditionsofitshistoricecosystem
mayexist within the colonized ecosystem. Thesepockets of habitat
canbethoughtofasanalogstothehistoricecosystemofthecoloniz-
ingspecies.Thus,weadopttheterms“habitatanalog”and“analogous
habitat” from the urban and reconciliationecology literature (sensu
Lundholm& Richardson,2010).Habitatanalogs havereceivedsome
attentionasartificialhabitatsfoundinhighlyalteredecosystemsthat
replicateconditionsexperiencedbyspeciesintheirnativeecosystems
(Lundholm&Richardson,2010andreferencestherein).Thesehabitats
rangefromquarries(Tropek&Konvička,2008;Tropeketal.,2010)to
urbanrubble (Grant, 2006) and oftenprovidehabitat and refugefor
speciesthatcouldnototherwisethriveinthesurroundingecosystem
(Chester&Robson,2013;Lundholm& Richardson,2010). Whilethe
termshabitatanalogandanalogoushabitathavepredominantlybeen
usedtorefertothosehabitatsfoundwithinhighlyalteredecosystems,
theterminologyisdirectlyapplicabletopatchesofhabitatwithinnat-
ural,butsuboptimal,colonizedecosystemsthatmorecloselyresemble
the historic ecosystem ofthe colonizer. Whether naturalor anthro-
pogenic,analogoushabitatsand otherrefugesmayprovide benefits
suchasamorefavorablethermalenvironment(Mosedale,Abernethy,
Smart,Wilson, & Maclean,2016;Wilsonetal., 2015), predation ref-
uge (Dumont, Harris, & Gaymer,2011), and higher quality foraging.
Anyofthesebenefitscouldhelpaspeciespersistorexpandmorerap-
idlyintoanotherwisesuboptimalecosystem.Thus,thesehabitatana-
logshavethepotentialtoplayacrucialroleincurrentandfuturerange
shifts.However,theimpactofanalogous habitats and other refuges
onrange-shiftingspecieswithincolonizedecosystemsisrelativelyun-
derstudied(butseeWilsonetal.,2015).
ThemangrovetreecrabAratus pisoniioffersanideal opportunity
toexamine the impacts ofboth a colonizedecosystemand a poten-
tialanalogoushabitatonarange-shiftingspecies.Thisarborealcrabis
historicallyassociatedwithNeotropicalmangroveforestsdominated
bythered mangroveRhizophora mangle(Wilson, 1989).However,its
climate-mediated northward range expansion has recently outpaced
thatofthe mangrove ecosystemresultinginthe colonizationofsalt
marshesin the southeastern UnitedStates (Riley,Johnston,Feller,&
Griffen,2014).Thesaltmarsh,whichisdominatedbythegrassSpartina
alterniflora,differsgreatlyfromthe mangroveforestswhereA. pisonii
hashistoricallybeen found.Themangroveprovidesashadedhabitat
withtallverticalstructureandeasyaccesstotheprimaryfoodsource
ofA. pisonii,R. mangleleaves(Beever,Simberloff,&King,1979;López
&Conde,2013),whichareabsentinthesaltmarsh.Thus,A. pisoniiin
thesalt marshfindthemselves inanecosystemwhich differsgreatly
in structure and foragingopportunities from that to which they are
adapted.As a result,A. pisoniiinthesaltmarshdisplaysmaller body
sizes,smallerclutch sizes, and lower larval quality than conspecifics
in the mangrove(Riley & Griffen, 2017). Thus, it appears that com-
paredtothehistoricmangrove,thesaltmarshisasuboptimalhabitat
for A. pisonii. However,A. pisonii is alsofoundon the anthropogenic
habitatofdockswithinthesaltmarsh.
Analogoushabitatsconferbenefitsonaspeciesbybeinginsome
way similar to its historic ecosystem. Docks may fit this criterion
withinthesaltmarsh astheyprovideA. pisoniiwith ashadedhabitat
and vertical structuremore similar to the historic mangrove as well
aseasyaccesstofoodin theformofabundant foulingcommunities.
Whilemangroveleaves are not available in the dock habitat, animal
material,which isabundantondocks in the formoffoulingcommu-
nities,isahigh-qualityfoodsource(Riley,Vogel,&Griffen,2014)that
ispreferredbyA. pisoniiovermangroveleaves(Erickson, Feller,Paul,
Kwiatkowski,&Lee,2008).Easyaccesstoahigh-qualityfoodsource
couldbe a boon to A. pisonii as the quantity and quality ofdiet play
crucialrolesintheenergeticsandlifehistoryofanindividual(Charron
etal.,2015;Wen,Chen,Ku,&Zhou, 2006).The shadedhabitatpro-
videdbythe dock itself, which is similartothe shade providedbya
mangrovecanopy,maybeanadditionalbenefitasthethermalhabitat
experiencedbyanorganismhasadirectimpactonitsphysiologyand
lifehistory(Huey,1991;Leffler,1972), especiallywhenwarmerthan
optimal(Gillooly,Brown,West, Savage,&Charnov,2001). Thus, the
    
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CANNIZZO et Al.
structure,food,andshadeprovidedbydocksmayallowthemtopro-
videimprovedhabitat forA. pisonii withinthesuboptimal salt marsh.
The use of anthropogenic structures to provide favorable habitat
forspecies experiencing adverseeffectsof climate changehasbeen
proposed (Shoo etal., 2011) and implemented (Mitchell, Kearney,
Nelson,&Porter,2008)asanaspectofadaptivemanagement(Heller
&Zavaleta,2009). However,these structures havealwaysbeende-
signedtocounteractnegativeimpactsexperiencedbyspeciesineither
theirhistoricorhighlydegradedecosystems.Unliketheuseofshade-
clothshelters(Mitchelletal.,2008)andartificialburrows(Souter,Bull,
&Hutchinson,2004),docksrepresentananthropogenichabitatfound
in a colonized natural ecosystemthat was not intended to improve
habitatconditions.
Weexaminetheimpactofthesaltmarshanddockhabitatsoneco-
logicalandlifehistorytraitsofA. pisoniithatinfluencebothindividual
performanceandtheabilityofthisspeciestopersistandexpandinto
thesaltmarsh.This includes aspects of behaviorrelatedto diet and
energystorage, thermal conditionsexperiencedbyA. pisonii, andan
explorationofdietaryintakeandqualityineachhabitat.Wecompare
individualsfromthecolonizedhabitats(saltmarsh anddock)to each
other and to a baseline of conspecificsfrom the historic mangrove
ecosystem.Wetest the overarchinghypothesisthat, in each aspect,
A. pisoniifoundondockswithin thesaltmarshwillbemoresimilarto
conspecificsinthehistoricmangrovethantothoseinthesurrounding
saltmarsh.
2 | METHODS
2.1 | Study species
Aratus pisonii is a mangrove-associated crab found throughout the
Neotropics(Rathbun,1918;Warner,1967).Thislargelyarborealsem-
iterrestrial crab has an ecology that is closely tied to the mangrove
trees themselves (Beever etal., 1979; Warner, 1967). In fact, while
itwillfeed opportunistically on high-qualityanimalmaterial (Beever
etal.,1979;Ericksonetal.,2008),itsprimaryfoodsourceisfreshman-
grove leaves, specifically from the red mangrove R. mangle (Beever
etal., 1979; López & Conde, 2013). Individuals maintain strong site
fidelitytoindividualtrees,abehaviorlostinthesaltmarsh,fromwhich
theytend to moveonlya short distance(Cannizzo& Griffen, 2016).
Despitethis fidelity, this crab isnot aggressively territorial, it is not
uncommon to see numerous individuals in close proximity, and the
FIGURE1 Mapofthelocationofstudy
sites,northernmostAratus pisonii(Riley,
Johnstonetal.,2014),andnorthernmost
black(Avicennia germinans)andred
(Rhizophora mangle)mangroves(Williams,
Eastmanetal.,2014;Williams,Lundholm
etal.,2014).Themapalsodisplaysapoint
delineatedastheextentofthemangrove-
dominatedecosystem.Whilethetransition
frommangrovetosaltmarshexists
asamosaic-likeecotone,thislocation
representsanareawithroughly50:50
mangrove:saltmarshcoverage(Rodriguez,
Feller,&Cavanaugh,2016;ICFellerpers.
com.).Northofthisline,mangrovescan
stillbefoundbutareprogressivelymore
isolatedandexistasindividualsorsmall
patcheswithinasaltmarsh-dominated
ecosystem
4 
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   CANNIZZO et Al.
speciesmaintainsasizeandsex-basedsocialhierarchylargelythrough
ritualisticdisplays(Warner,1970).Further,thisspeciesislargelyter-
restrial,returningtothewateronlytowetitsgillsandreleaselarvae,
andeven exhibitsa characteristic climbingbehavior to avoidaquatic
predatorswhenthetiderises(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-
tatswerefound in the vicinity of Saint Augustine, Florida (Figure1;
TableS1).ThemangrovesitesarewithinthehistoricrangeofA. pisonii
(Rathbun,1918;Warner,1967), whilesalt marshanddocksitesrep-
resenthabitats within the recently colonized region (Riley,Johnston
etal.,2014).Thesiteschosenwereselectedastheyarerepresentative
oftheirrespectivehabitattype.Studiedsaltmarshsites werealways
atleast0.75kmfromthenearestdock to prevent the possibility of
examiningcrabsthathaveaccesstothedock habitat.Whiletwosalt
marshsitesandone docksiteweresouthof thenorthernmostman-
grove(Figure1),mangroves are scarce in this salt marsh-dominated
ecosystemandtendtoexistonlyinsmallisolatedpocketsofindividu-
als.Further,onlyonesiteofeachhabitatissouthofthenorthernmost
redmangrove, the species to which theecologyofA. pisoniiis most
closelytiedinthemangroveecosystem(Beeveretal.,1979;Warner,
1967).Whileitwasimpossibletoensurethattherewasnomovement
betweenthedockandsaltmarshforcrabsexaminedondocks,crabs
tendtoexhibitlittlemovementfromacentralforagingarea(Cannizzo
&Griffen, 2016). Further, evenifthere is some movement between
thehabitats,thiswouldresultinaconservativetestofourhypotheses
byminimizingobserveddifferences.
2.3 | Behavioral observations
Weobservedthebehaviorofindividualcrabsin situ.Ineachhabitat,
wecollected groups of five adult A. pisonii byhand and determined
thesexandcarapacewidth(tothenearest0.1mm)ofeachindividual.
Thegroupsofcrabsweremadeupofthefirstfiveindividualsthatwe
encountered and could capture and were drawn from all accessible
habitats. We then painted the carapace of each crab an identifying
colorwithnailpolishtoaidinidentificationand visibility.Preliminary
experimentsdeterminedthatpaintingthecarapacesofcrabsdidnot
alter their behavior or thermal properties. Following a short period
of observation to ensure normal behavior, we released the crabs
ontoa single tree within 10mof the collection tree of all individu-
als(mangrove), ontoseparateS. alterniflora stalkswithin10m ofthe
areaofcollection(salt marsh), or onto the same piling (dock) of the
dockwhere all individuals were captured. Releasingcrabsneartheir
capturelocation allowedforobservationwhile alsoensuringas near
anaturaldistributionofcrabsaspossible.Toavoidimmediateretreat
into holes, release in the salt marsh occurred during the rising tide
whenthecrabshadnoaccesstothesediment.
Inallhabitats,A. pisoniiclimbsstructureasthetiderisestoremain
outofthe waterandwill even leave occupiedsheltertodo so (per-
sonalobservation).Thus,weobservedcrabsinthemangroveandsalt
marshhabitats from the time they lost access to the sedimentuntil
the receding tide onceagain allowed access to the sediment (~6hr
depending on site and day). In contrast, in the dock habitat, crabs
generallylack access to the sediment throughout the tidal cycle. To
obtain an observational period similarto that of the other habitats,
wethereforeobservedcrabsondocksfrom3hrbeforeslackhightide
until3hrafterslackhightide.Wewatchedcrabsfromadistanceusing
binocularsto avoidimpacting theirbehaviorand monitoredthe indi-
vidualscontinuouslythroughouttheobservationalperiod.Theobser-
vationallocationwaschosen to maximizevisibility,andthe observer
wasfree to move if increasedvisibility was necessary.Behaviorwas
recordedevery 5min and at every change in behaviorwithin those
5-min intervalsasone offour categories:feeding, sitting,moving,or
not-visible (Table1).Each group offivecrabs was only observed for
behavioronce,andonlyonegroupofcrabswasobservedonanygiven
day.AllobservationsoccurredfromMaythroughAugust.
Weseparated the observations into ebb and flood tidal periods
to examine differences in foragingbehavior as crabs gained or lost
accesstofoodsourcesonthesedimentandwethabitatstructure.To
avoidbiasingthedatawithcrabsthatwerenotvisibleforlongperiods,
wealsoremoveddatafromindividualsthatwerenotvisible formore
than66%ofthetidalperiod.Thiscorrectionresultedin theobserva-
tionof38, 55, and 39 individuals duringflood tide and 41, 54, and
39individuals duringebb tide inthe mangrove,salt marsh,anddock
habitats,respectively.Unlessotherwisestated,theseindividualcrabs
weretreatedasthereplicatesforallassociatedstatisticalanalyses.
To test for the effects of multiple biological and environmental
variablesontheproportionoftimespentfeedingduringfloodorebb
Behavior Description
Feeding Thecrabisobservedactivelymovingitsclawsfromafooditemorsubstratetoits
mouth.
Moving Thecrabisactivelymovingalongasubstrateandnotfeeding.Otherenergy-
expendingnonfeedingactivities,suchasritualaggression,werealsoclassified
undermovingastheyrepresentanexpenditureofenergy.However,these
activitieswererareandshort-lived
Sitting Thecrabisnotactivelymoving,feeding,orparticipatinginanyactivity
Not-
visible
Thecrabisnotvisibletotheobserver
TABLE1 Ethogramdescribingthe
behavioralcategoriesassignedwhile
observingAratus pisonii
    
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 5
CANNIZZO et Al.
tide,weranageneralizedlinearmixedmodelwithabinomialerrordis-
tribution.We included carapacewidth,sex,habitat,airtemperature,
andtide(ebborflood) asexplanatoryvariables.Wealsoincludedthe
individualcrabIDasarandomfactortoaccountforthemultipleobser-
vationsofindividualcrabs(ebbandfloodtide)andweightedthemodel
bythe total time ofobservation for eachindividual.Additionally,we
exploredtheproportionoftimeA. pisoniispentmovingbyemployinga
similargeneralizedlinearmixedmodelbutwiththeproportionoftime
individualsspentmovingastheresponsevariable.
2.4 | Exposure to thermal microhabitats
To explore the thermal conditions experienced by A. pisonii in each
habitat,we compared the solar exposurethey experienced. We did
thisby recording thepositionof crabs as insunor shade duringthe
behavioralobservationsdescribedabove andcalculatingthe propor-
tionof time they spentinthesun. To confirm theinherentassump-
tionthatindividualsexperiencehighertemperatureswhileinthesun,
weplacedHOBO thermal data loggers underneath a dock, and in a
nearbysaltmarshatthesamesiteattachedtoawoodendowelhigh
enough to remain out of the water. These loggers simultaneously
gatheredtemperaturedataeveryminute fromnoon on8 September
2016tonoon on11September2016.Theloggerdatawerenot col-
lectedcoincident with observations of crabsas it was not intended
to measure the exact temperatures crabs experienced but relative
differences between temperatures in the sun and shade. While we
tookadvantage ofthestructural differences betweenthesehabitats
toobtaindatapertainingtotemperatureexposurewhilecrabsarein
thesun(saltmarshlogger)and shade (dock logger), these measures
donot necessarily represent the thermal conditions experiencedby
allcrabs ineachof the twohabitatsat all times.Rather,as the dock
andmangroveprovide shadedcanopies andthe saltmarshdoesnot,
they represent the difference in the thermal conditions most often
experiencedbythecrabsineachhabitat.
To further examine the thermal habitat experienced by the ob-
servedcrabs,weusedaFLIRinstrumentsC2compactthermal imag-
ingcameratotakeathermal imageofeachvisiblemarkedcrabevery
15min throughout the observational period. The days when crabs
were observed took place over a wider range of air temperatures,
which was measuredon site, in the mangrove and salt marsh habi-
tatsthanondocks.Thus,toavoidtheconfoundingfactorofrelatively
coolerairtemperaturesinthesehabitats,onlythermalpicturestaken
ondayswhichhadanaverageairtemperature>29°Cwereexamined.
Thistemperaturerepresentedthelowerboundofairtemperatureson
days crabswere observed in the dock habitat. Alongwith the elim-
inationofphotographswhere no crabswerevisible, thisresultedin
theanalysisof455,294, and289thermalphotographsfromthe salt
marsh,mangrove,anddockhabitats,respectively.Wethenemployed
theprogramFLIRtoolstoobtainthetemperatureatthecenterofthe
carapaceofeachcrab.
We suspected that the proportion of time crabs spent in both
thewater and thesunwouldimpact their body temperature,sowe
calculated these valuesfor all individuals for which we had thermal
photographs.We compared thesevalues between habitats using an
ANOVA followed by aTukey’s HSD test for multiple comparisons.
Unlessotherwise stated, weimplementedthisstatisticalmethod for
allsubsequentcomparisonsmadebetweenandwithinhabitats.
To explore the factors that influence crab temperature, we av-
eraged the recordedbody temperature of individual crabs over the
courseofanobservationalperiod.Weexpected thatthesolar radia-
tionexperiencedbycrabsoverthecourseofanobservationalperiod
(~6hrdependingonsite andday)wouldimpacttheirbodytempera-
ture.Thus,toexaminetheimpactofsolarexposureoncrabtempera-
ture,weobtainedshort-andlong-wavesolarradiationfromtheNCEP
NorthAmericanRegionalReanalysis(NARR).NARRhasaresolutionof
32kmandcalculatessolarradiationin3-hrintervals.Weobtainedthe
solarradiationatthe gridpointclosesttoeachsiteand averagedthe
sumoftheshort-andlong-wavesolarradiationovertheobservational
period.Thisnumber,inW/m2,wasthenmultiplied bythe numberof
secondsthe crabwas observedtospend in thesunto obtainarela-
tivemeasure ofthe solar energyexperienced overthe observational
period.Thiscalculatedvariablewillhereafterbereferredtoas “solar
exposure”.Wethenranamixedeffectslinearmodelwithhabitat,pro-
portionoftimeinwater,solarexposure,andambientairtemperature
asexplanatoryfactorsfortheaveragedcrabbodytemperatures,which
wereincluded asthe responsevariablein the model. Wealso ran a
similar model with the averagedifference between crab body tem-
perature and the ambient airtemperature as the response variable.
Thismodel allowed us toanalyzethe ability ofcrabsin each habitat
tomaintaina bodytemperaturecoolerthan ambientand explorethe
factorsthatimpactthisability.Inbothmodels,thecontinuousexplan-
atoryvariableswerez-scoredtofacilitatecomparisonoftheirrelative
impactsonthe responsevariable.Duetothesite-fidelitybehaviorof
A. pisonii(Cannizzo& Griffen,2016), somecrabswerephotographed
on multiple days. Thus, to accountfor these multiple observations,
crabIDwasincludedinthemodelsasarandomfactor.Thesemodels
allowedustoexploretheimpact ofthese factorsonboth crabbody
temperaturesandcoolingonthetimescale onwhich theexplanatory
factors wereavailable and meaningful. Finally, we ran linearregres-
sionstodeterminewhethertherewererelationshipsbetweenthepro-
portionof timeindividualsspent in thewaterand sunaswell asthe
timespentinwaterandsolarexposure.
2.5 | Diet and energy storage
Toexamine diet indices and the investment of A. pisonii into energy
storage,we collected individuals from each habitatduring the sum-
mersof 2015 and 2016.Oneachof nine randomly selected daysin
eachhabitat,15individualadultA. pisoniiwerecollectedbyhandand
immediately placed on dry ice. In the mangrove and salt marsh, we
collectedthesecrabsinthreegroupsoffiveatthreedistincttidalpe-
riods: just after losing access to the sediment on the flood tide, at
slackhightide,and just before regaining access to the sediment on
theebbtide.Thisresultedincollectiontimes~3hr apart.Duetothe
constantlackofaccesstosedimentinthedockhabitat,wecollected
crabs3hrbefore,at,and3hrafterslackhightide.Asinthebehavioral
6 
|
   CANNIZZO et Al.
observations, the first five crabs we encountered were collected at
eachof these tidalperiods.Thiscollection regime resulted inatotal
of135crabsfromeachhabitat(45fromeachtidalperiod)whichwere
kept frozen until dissection. No measured indices differed between
years,andthus,datawerepooledacrossyearsforanalysis.
Based on preliminary observations in the laboratory, the gut
clearancetime ofA. pisonii is ~3hr.Therefore,our collection regime
allowedfortheanalysisofdietwhencrabshadaccesstothesediment
(collectedon the flood tide), when crabs only had access to unsub-
mergedhabitat(collectedatslack hightide),andwhen crabshadac-
cesstorecentlysubmergedhabitat(collectedontheebbtide).Priorto
dissection,wedeterminedthesexandcarapacewidth(tothenearest
0.1mm)ofeachcrab.
We ascertainedthe gut fullness of each crab to obtain a snap-
shot of the quantityof food consumed during each tidal period by
removingthe gut contentsanddrying them at 60–70°C to constant
weight.Westandardizedgutfullnessbydividingthe massofthegut
contentsbythevolumeofthegut(
V=
a
(212)×Gut width3
,where
aisa correctionfactorof0.92forcrabs[Griffen&Mosblack,2011]).
Wethenemployeda two-wayANOVAtocompare the standardized
gutfullness betweentidal periodswithinand betweenhabitats.Due
to inclement weatherduring one observation day in the dock habi-
tat,crabswerecollectedwithout regardfortidalperiod.Thisleadto
only120crabsfromthedock,40pertidalperiod,beinganalyzed for
gutfullness.Asthiswastheonlydissectionparameterdependenton
timeofcollection (seebelow),onlygutfullnesswasimpactedbythis
reducedsamplesize.
Inadditiontodietquantity,weexploredlong-termdietqualityby
measuring the cardiac stomach ofeach crab to the nearest 0.1mm
andcomparingthe gut-width:carapace-widthratio betweenhabitats.
Incrabs,thisratioisaproxyforlong-termdietqualitywithasmaller
ratiocorresponding toahigherquality dietthatlikelycontainsmore
animalmaterial(Griffen&Mosblack,2011).
Toexaminetheproportionalenergeticinvestmentintoenergystor-
agebyconspecificsineachhabitat,weseparatedanddriedtheprimary
energy storage organ(hepatopancreas) (Parvathy, 1971) and the so-
matictissue of each crab. Tocompareenergetic investment between
habitats,wecalculatedthehepatosomaticindex (HSI)ofeachcrabas
the ratio of the dryweights of the hepatopancreas and the somatic
tissue, which is a common measure ofenergy stores in crustaceans
(Griffen,Vogel,Goulding,&Hartman,2015;Kennish,1997;Riley,Vogel
etal.,2014; Sánchez-Paz,García-Carreño,Hernández-López, Muhlia-
Almazán, & Yepiz-Plascencia, 2007). However, HSI is dependent on
bothsex and reproductivestage (e.g.,afemalewill have a lower HSI
whencarryingeggs;Belgrad,Karan,&Griffen,2017).Thus,wegrouped
crabsas male, gravid female, or nongravid female and comparedthe
HSIofthesegroupsbetweenhabitats.Duetoaproblemintransporta-
tion,thelegsofcrabsfromtwotidalperiodsononedayfromtheman-
grovebecamedetachedandmixed.Thismadeitimpossibletoreliably
obtainaweight for somatic tissue from these 10 crabs resulting in a
reducedsamplesizeof125crabsfromthemangroveanalyzedforHSI.
Asthiswastheonlyparameterthatincorporatedsomaticweight,itdid
notaffectthesamplesizeofanyotheranalysis.
2.6 | Statement of animal rights
Allapplicableinstitutionaland/ornationalguidelinesforthecareand
useofanimalswerefollowed.
3 | RESULTS
3.1 | Demographics
Aratus pisonii in the salt marsh habitat were smaller
(CW±SD=12.97±1.57mm) than conspecifics in the mangrove
(17.95±3.12mm) and dock (17.83±2.09mm) habitats (ANOVA,
F2=314.9, p<.001; Tukey’s HSD, p<.001, FigureS1). However,
individuals found in the dock habitat did not differ in size from
conspecificsinthemangrove(Tukey’sHSD,p=.850,FigureS1).
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
notdifferbetweenthe dockandsalt 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),butincreasedasthetidefellandforagingonrecentlysub-
mergedstructurebecamepossible(GLM,estim.=1.460,z=43.28,
p<.001).Timespentfeedingalsodifferedwithinhabitatsandwas
contingent on the tidal period (two-way ANOVA, Habitat×Tide,
F2=8.664,p<.001; Tukey’s HSD, p<.05, Figure2). Additionally,
foraging depended on interactions between the tide and habitat.
Afterslacktide,crabsinthesaltmarshexhibiteda1.4-foldgreater
increase in feeding than crabs on docks (GLM, estim.=3.975,
z=3.63,p<.001)and a 5.7-fold greaterincreasethan conspecif-
icsinthemangrove(GLM,estim.=4.655,z=4.76,p<.001),while
theincreaseinfeedingduringthis 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
feedingdifferently between habitats. Individualsinthe dock habi-
tatincreasedtheproportion oftimetheyfedastemperaturesrose
(GLM, estim.=0.526, z=8.74, p<.001; FigureS2), while the op-
positewas observedinboth the mangrove(GLM,estim.=−0.525,
z=−8.73p<.001)andsaltmarsh(GLM,estim.=−0.330,z=−2.22
p<.001)drivingtheoverallnegativeimpactoftemperatureontime
spent feeding. Additionally, the interaction between temperature
andhabitatrevealedthatthisreductioninfeedingwith increased
temperature was greater in the mangrove than in the salt marsh
(GLM,estim.=0.195,z=3.24p=.002).
    
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CANNIZZO et Al.
Movementpatternswere similarto those seen infeedingas the
proportionof time A. pisonii spent movingwasnotcontingent upon
individual size or sex (GLM, estim.=−0.021, z=−0.74, p=.458;
estim.=0.148,z = 1.003 p=.316,respectively),butwasimpactedby
environmental factors. However, in contrast to feeding, movement
decreasedduringebbtide(GLM,estim.=−0.206,z=−4.46p<.001)
andincreasedwith 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-
ferbetweenthesaltmarshanddockhabitats(GLM,estim.=−0.293,
z=−1.73p=.084).Theinteraction betweenmovement andtidere-
vealedthatindividualsinthedockhabitatincreasedtheproportionof
timetheymovedafterslacktide(ebbtide)asopposedtothedecrease
inmovement inboththe mangrove(GLM,estim.=−3.658, z=2.49,
p=.021) and salt marsh (GLM,estim.=−6.110, z=−3.44, p<.001)
which drovethe overall negative trend of reducedmovement after
slacktide.However,thedecreaseinmovementduringebbtidedidnot
differbetweenthemangroveand saltmarsh(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,Figure3a) and more than 18-foldless time in thesunthan
conspecifics in the salt marsh (ANOVA, F2=110.5 p<.001; Tukey
HSD, p<.001, Figure3a). This likely resulted in individuals in the
mangrove and dock habitats experiencing a cooler microhabitat, as
temperaturesrecorded duringtheday were asmuchas 10°C cooler
intheshadeof adockthan inthenearbysaltmarsh (Figure3b).We
confirmedthisconclusionthroughtheanalysisofcrabbodytempera-
turesobtainedfromthethermalphotographs.
Habitatplayedanimportantroleindeterminingcrabbodytempera-
ture.Crabsinthesaltmarshhadhigherbodytemperaturesthanthose
found in the dock and mangrovehabitats (LMER, estim.=−1.1272,
t98=−2.473 p=.0151; estim.=−1.8366, t90=−3.63, p<.001,
respectively; Figure4a). These individuals were also less able to
maintaina body temperature coolerthan 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; Figure4b).Additionally, compared to conspecifics in the
mangrove,crabs in the dock habitathad ahigherbodytemperature
(LMER,estim.=−0.7095,t64=−2.427 p=.0181) and werelessable
to maintain a body temperature cooler than the ambient (LMER,
estim.=−0.7180, t68=−2.56 p=.0126). The temperature of crabs
FIGURE2 Theproportionoftimespentfeeding±SEbyAratus
pisoniiinthemangrove,saltmarsh,anddockhabitatsbeforeand
afterslackhightide.Groupsthataresignificantlydifferentare
denotedbydifferentletters
FIGURE3 (a)Boxplotscomparingtheproportionoftimespent
insunbyAratus pisoniibetweenthethreehabitats.Groupsthatare
significantlydifferentaredenotedbydifferentletters.Ineachbox
plot,andinallotherboxplotsrepresentedinthispaper,themedian
isrepresentedbyaheavyline,theboxrepresentstheupperand
lowerquartiles,whilethewhiskersrepresent95%ofthedataand
circlesshowoutliers.(b)Thermalloggerdataofloggersplacedinthe
shadeunderadock(dashedline)andintheopeninthesaltmarsh
(solidline)from8September2016to11September2016
8 
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   CANNIZZO et Al.
alsoincreasedwithambient airtemperature (LMER,estim.=0.9765,
t99=8.99p<.001)anddecreasedas a crab spent a greater propor-
tion of its time in the water (LMER, estim.=−2.4725, t98=−2.21
p=.0295).However,theamountofsolarexposureacrabexperienced
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 temperaturesprogressively cooler than ambient as the
ambienttemperatureincreased(LMER,estim.=−0.7839,t105=−7.51
p<.001), as solar exposure increased (LMER, estim.=−0.4262,
t105=−2.23p=.02813), and as crabs spent more time in thewater
(LMER,estim.=−2.6752,t104=−2.47p=.0152).Further,crabsinthe
saltmarsh spentagreaterproportionoftheir timeinthe waterthan
conspecifics in the mangrove (ANOVA, F2=8.813, p<.001; Tukey
HSD, p<.001; FigureS3)and dock habitats (TukeyHSD, p = .0087;
FigureS3)which did not differinthisregard(TukeyHSD, p = .0732;
FigureS3).Thisisofnoteastherewasapositiverelationshipbetween
thetime a crab spent in thewaterand both thetimeitspentin 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, FigureS4) and tidal period
(two-way ANOVA, F2=15.38, p<.001). In particular, the interac-
tionofhabitatandtidalperiod(two-wayANOVA,F4=5.18,p<.001)
suggeststhat gutfullnesswas dependentona combinationofthese
variables.Whenanalyzedbyhabitat,itisclearthatA. pisoniiwereable
tomaintainaconsistentgutfullnessthroughoutthetidalcycleinboth
themangrove(TukeyHSD,p>.50;Figure5)anddockhabitats(Tukey
HSD p>.50; Figure5). However, despite an overall higher gut full-
ness(Tukey HSD, p<.001, FigureS4), crabsin the salt marsh were
unable to maintain a full gut and thus were likely unable to obtain
sufficientfood,duringthetimewhenthe rising tide restricts access
to food found on the sediment or deposited by water on structure
(Tukey HSD, p<.001; Figure5). During other times in the tidal
cycle,however, crabs in the salt marsh maintainedahighergutfull-
nessthan conspecifics in the mangrove and dock habitats (two-way
ANOVA, F4=5.18, p<.001; Tukey HSD, p<.01; Figure5). In addi-
tion to unreliable foraging, A. pisonii in the salt marsh had a higher
FIGURE4 (a)Averagebodytemperature±SEofcrabsin
eachhabitat.Groupsthataresignificantlydifferentaredenoted
bydifferentletters.(b)Differencesbetweenaveragecrabbody
temperatureandambientairtemperature±SEineachhabitat.
Groupsthataresignificantlydifferentaredenotedbydifferentletters
FIGURE5 BoxplotsshowingthegutfullnessofAratus pisoniiby
tidalperiodinthemangrove,saltmarsh,anddockhabitats.Groups
thataresignificantlydifferentaredenotedbydifferentletters
    
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CANNIZZO et Al.
gut-width:carapace-width ratio, indicating a lower quality long-term
diet,thanconspecificsineitherthehistoricmangroveordockhabitat,
wheredietqualitywashighest(ANOVA,F2=20.52,p<.001;Tukey’s
HSD,p<.05,Figure6).
Proportionalenergetic investment into energy storage (HSI) was
highestinthemangroveforbothmales(ANOVA,F2=23.27,p < .001;
Tukey HSD, p<.001) and gravid females (ANOVA, F2=29.24,
p<.001; Tukey HSD, p<.001, Figure7). Energy storage was also
greateringravidfemalesinthesaltmarshthanondocks(TukeyHSD,
p<.001,Figure7),but did notdiffer between these two habitats in
males (TukeyHSD, p=.065, Figure7). In nongravid females, energy
storagewaslowestinthedockhabitat(ANOVA,F2=36.13,p < .001;
TukeyHSD, p<.001, Figure7) but did notdifferbetween theman-
groveandsaltmarsh(TukeyHSD,p=.060,Figure7).
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,thisstudysuggeststhattheroleofthedockhabitatin
providingimproved conditionsforA. pisonii within thecolonizedsalt
marshecosystemismixed.Yet,whiledocksdonotprovideimproved
conditionsineveryway,theydoappeartoprovideimprovementsfor
anumberofimportantaspectsofthiscrab’secologyandphysiology.
Oneimportant benefitconferredby docks islargerbody size. While
thereisasyetnoreliablewaytoagethesecrabs(Hartnoll,2001;Vogt,
2012),andthusnowaytodeterminetherelativeimpactsofageand
growthrate,alargerbodysizeisoftenbeneficial.ForA. pisonii,larger
size confers benefits through size-specific dominance hierarchies
(Warner, 1970) and increased reproductive output (Riley & Griffen,
2017),whichinturn benefitsthepopulation. Thus,greatersize isan
exampleofanindividualbenefitprovidedbyananalogoushabitatthat
mayhavecascadingbenefitsforarange-shiftingspecies.
Understanding how analogous habitats confer general benefits,
suchaslargersize,requiresanunderstandingofthemechanismsthat
leadtothosebenefits.Thiscanbeexploredthroughtheexamination
oftheprecisewaysinwhich ananalogoushabitatprovidesimproved
conditions.Forexample,thequantityandqualityofanindividual’sdiet
haveadirectimpact onseveralaspects ofitsecologyandlifehistory
includinggrowth(Buck etal.,2003; Griffen,Guy,& Buck,2008), off-
spring quantity and quality (Green, Gardner, Hochmuth,& Linnane,
2014;Millamena&Quinitio,2000),andbioenergetics(Charronetal.,
2015;Riley,Vogeletal., 2014).Thus,an improveddietmayitselfbe
themechanismbehind otherbenefitsincludingincreasedsize.Docks
clearly provide improved diet and foraging conditions to A. pisonii
through more continuous accessto a higher quality diet than else-
whereinthesalt marsh.However,thehighgutfullness displayedby
crabs in the salt marsh when the sediment is accessibleand during
ebb tide suggests that they exhibit compensatory feeding through
increasedconsumption when foodis available.While compensatory
feedingis commonamong individuals facedwith poordiets,it isnot
alwayseffective (Cruz-Rivera & Hay,2000) and may be hindered by
irregularaccesstofoodinthesaltmarsh.Inadditiontoregularaccess
tofood,docksprovideabundantanimalprotein,ahigh-quality food
(Riley,Vogeletal.,2014),intheformofhigh-densityfoulingcommu-
nities.We regularlyobservedA. pisoniifeedingonfoulingorganisms
suggesting that animal material plays an important role in the im-
proveddietqualityofthesecrabs.
FIGURE6 Boxplotscomparingthegut-width:carapace-width
ratiosofAratus pisoniibetweenthemangrove,saltmarsh,anddock
habitats.Groupsthataresignificantlydifferentaredenotedby
differentletters.Alowergut-width:carapace-widthratiosuggestsa
relativelyhigherproportionofanimalmaterialinthelong-termdietof
theindividual
FIGURE7 Boxplotscomparingtheinvestmentinlong-term
energystorage,calculatedashepatosomaticindex,ofmale,gravid
female,andnongravidfemaleAratus pisoniibetweenthethree
habitats.Groupsthataresignificantlydifferentaredenotedby
differentletters
10 
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   CANNIZZO et Al.
Similarlytodiet,thethermalconditionsexperiencedbyanorganism
greatlyimpactitsphysiologyandlifehistory(Huey,1991;Leffler,1972).
Thus,improvedthermalconditionsareapotentialmechanismthatcould
leadto otherbenefitsincluding largersize(Huey,1991; Leffler,1972).
ForA. pisonii,docksprovideashadedthermalrefugewhichallowscrabs
tomaintainabodytemperaturethatislower,andlowerthanambientto
agreaterextent,thanconspecificselsewhereinthe saltmarsh.Infact,
theextensive use of shaded areasofthe dock and mangrovehabitats
suggeststhatshadedareasarepreferredbyA. pisoniiandtheexcessive
timeconspecificsfrom thesalt marshspend inthe sunis likelyaresult
ofthehabitatstructure,notpreference.Theuseofthermallysheltered
habitatsinsuchareaswherepreferredthermalconditionsarenotreadily
availableisaprimarywayinwhichspeciesmayaddressregionalclimatic
shifts(Williamsetal.,2008).Whilewefocusedontheabilityofdocksto
providecrabsa coolerhabitat duringsummer months,the abilityofan
analogoushabitattoprovidea warmer microhabitat in winter months
couldalsobevitaltoarange-shiftingspecies.
Despite the cooler conditions providedby docks, the thermal dif-
ferences observed between habitats were less than the disparity in
timespentinthesunwouldsuggest. Onepossibilityisthatcrabsinthe
open-structured salt marsh experience greater convective coolingdue 
to increased wind exposure(Ortega, Mencia, & Perez-Mellado, 2017).
However, our resultssuggest that the lower than expected body tem-
peratureofcrabsinthesaltmarshismorelikelyaresultofdifferencesin
thermoregulatorybehavior.Crabsinthesaltmarshappeartothermoreg-
ulatebydipping inwatertocoolthemselvesafterextendedtimein the
sun,aconclusionsupportedbythepositiverelationshipbetweentimein
waterand solar exposure. Indeed, a comparison of the z-scoredmodel
estimatessuggests thatthetime crabsspendin thewaterhas thelarg-
estimpact on boththeirbodytemperatureandtheirabilitytomaintain
abodytemperaturecoolerthantheambient air.Additionally,dippingin
watercouldhaveanadditionalcoolingeffectevenafterthecrabemerges
via evaporative cooling(Eshky, Atkinson, & Taylor, 1995), which could
alsobefurtherenhancedbyincreasedwindexposure.Indeed,incombi-
nationwiththeresultthatcrabsspendmoretimeinthewaterwhenex-
periencinggreatersolarexposure,itispossiblethatthiscouldexplainthe
unexpectednegativeeffectofsolarexposureonthedifferencebetween
crabbodytemperatureandtheambientairtemperature.Thus,whileex-
posuretothesunsurelyhasanacutewarmingimpact oncrabs, itssta-
tisticalimpactislikelyoverpoweredbytheimpactofcoolingwithwater.
The change in thermoregulatorybehavior in the salt marsh sug-
gestsanotherwayinwhichanalogoushabitatsmayprovideimproved
conditions in colonized ecosystems:by allowing individuals to avoid
potentiallycostlychangesinbehavior.Whilebehavioralchangesoften
provide the first response to alteredenvironments (Gross, Pasinelli,
&Kune, 2010; Sih,Ferrari,&Harris,2011; Wong& Candolin, 2015),
theycan lead to costly ecological trade-offs. ForA. pisonii, the need
to thermoregulate may require crabsto temporarily abandon forage
orshelter to move to waterwheretheyare likely exposed to higher
predation (Warner, 1967; Wilson, 1989). In fact, previous work sug-
gestedthatpredationon largeindividuals may be lower in the man-
grovethan the saltmarshwhich may contributetothesizedisparity
betweenthetwohabitats(Riley&Griffen,2017).Itispossiblethatthe
riskofpredationforlargeindividualsisalsolowerondocks,particularly
consideringthelowoccurrenceofsmallindividuals(FigureS1),further
contributing to the larger size of individuals found there. However,
while docks mayallow A. pisonii to avoid risky thermoregulatorybe-
havior,crabs found there exhibit foraging behaviorthat differs from
crabsin themangroveand issimilarto conspecificselsewherein the
salt marsh. Crabs in the dock and salt marsh habitats increasetheir
feedingas thetidefallssuggestingtheyfeed heavily on food that is
eitherdeposited on structureor submerged at high tide. This differs
fromconspecificsinthehistoricmangrovewhichfeedoncontinuously
accessiblemangroveleaves.Like dippinginwater to thermoregulate,
following recedingwater to feed may increase the risk ofpredation
byaquatic predators (Warner,1967; Wilson, 1989).Thus, the ability
ofdocks to allow A. pisonii to avoidpotentiallydangerous behavioral
changesismixed.
Foraging behavioris not the only way docks fail to provideim-
provedconditionsforA. pisonii.Inparticular,theproportionofenergy
stored by crabs in the three habitatsdiffered in unexpected ways.
Whilethe investmentintoenergystorage(HSI) waslower inthe salt
marshthan the historic mangrove habitat, it was lower still in crabs
foundon docks.Thisisparticularly perplexing whenconsideringthe
larger size and improved diet of crabs on docks. It is possible that
thedifferencesin diet observedbetweenhabitatsplaya rolein the
ability of A. pisonii to convertconsumed energy into stored energy.
Alternatively, some unknown energeticexpense or trade-off in the
dockhabitat maylead to adecreasein energystorage. Inanyevent,
the energystorage of A. pisonii warrants further studyand suggests
thatcrabson the docks likely have differentpatternsofenergyuse
thanthose in thesurroundingsalt marsh ecosystem.Given the met-
aboliccostsforcrabs ofstoringlipids inthe hepatopancreas(Griffen,
2017),the lower HSI seenincrabsonthe docks could be beneficial
forindividualsandmayreflectimprovedenergeticefficiencyforcrabs
usingthishabitattype.
While docks appear to provide several important benefits to
A. pisonii in the colonized salt marsh ecosystem,their role as an ana-
logtothe mangroveis clearlymixed.Yet,whatdocks dorepresentis
arelativelyunderstudied aspectofrangeshiftecology: theroleofan-
thropogenic habitat analogs in providing improved conditions within
suboptimalcolonizednaturalecosystems.However,anumberofstudies
haveproposedimplementingartificialhabitats,orhabitatmodification,
to minimize the exposure ofvulnerable species to stressful changing
conditionsintheirhistoricecosystems(Shooetal.,2011;Williamsetal.,
2008).Suchproposalshaveincludedinstallingmicrohabitatrefugesand
sprinklers foramphibians (Shoo etal., 2011), artificial breeding struc-
tures(Shooetal.,2011),shadecloths(Mitchelletal.,2008),andgeneral
habitat restoration using artificial structuressuch as burrows (Souter
etal.,2004)andformedconcrete(Webb&Shine,2000).However,the
useofanthropogenichabitatsinnaturalecosystemsthataspecieshas
neverbeforeinhabitedhasgarneredlittlediscussion.
The construction of artificial habitatsin unsuitable ecosystems to
help/encouragerange shifts has received some discussion as a facet
of adaptive management strategies (Hoegh-Guldberg etal., 2008).
Additionally,therehasbeenarobustdiscussionoftheuseofcorridorsto
    
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CANNIZZO et Al.
aidspeciesintheirclimate-inducedrangeshifts(Hannah,2001;Krosby
etal.,2010).Infact,increasingecologicalconnectivitythroughcitiesand
otherunfavorablehabitats to encouragethe movementofspecies be-
tweennaturalareashasbeenidentifiedascriticaltotheabilityofmany
species to persist in the face of changing climatic conditions(Krosby
etal., 2010; Williams, Eastman etal., 2014;Williams, Lundholm etal.,
2014).Suchdiscussionstendtofocusoncreatingorpreservingnatural
corridorsbetweennaturalareas(Hannah,2001;Krosbyetal.,2010).In
contrast, anthropogenichabitat analogs may increase, ratherthan im-
pede,the successand rateof rangeshifts. Whilethere hasbeensome
exploration of green roofs (Williams, Eastman etal., 2014; Williams,
Lundholm etal., 2014 and references therein), gardens (Goddard,
Dougill,&Benton,2010),street-sidevegetation(Swan,Pickett,Szlavecz,
Warren,&Willey,2011),andotheranthropogenic“stepping-stone”ref-
uges(Chester&Robson,2013;Gledhill,James,&Davies,2008;Santoul,
Gaujard,Angélibert,Mastrorillo,&Céréghino,2009)infacilitatingmove-
mentthroughcitiesandotherunfavorablehabitat,thisworkhaslargely
focusedonbiodiversityconservationandmovementbetweenhabitable
areasas opposed to rangeshifts (but see Grant, 2006).Yet,anthropo-
genicstructures which werenotspecificallydesigned as habitat could
increase the permeabilityof the habitat matrix during range shifts by
providingmorefavorablehabitatthanthesurroundingecosystem.Even
ifanthropogenichabitatanalogsdonotincreasetherateofarangeshift,
theirabilitytoprovideimprovedconditionscouldprovevitaltothesuc-
cessofrange-shiftingspeciesincolonizedecosystems.
Asclimate changecontinuesto forceor encouragespecies to colo-
nizenewecosystems,itwillbeincreasinglyimportanttounderstandhow
theseshiftingspeciesareimpactedbyhabitatswithwhichtheyhaveno
ecologicalorevolutionaryexperience.Theroleofanthropogenichabitats
ashabitatanalogsmayplayacrucialroleinthe outcomeofrangeshifts.
Thus,theexistenceofanthropogenichabitatanalogsshouldbeincluded
inanalysesofthevulnerabilityofspeciestoclimatechange(seeWilliams
etal.,2008foraframeworkforsuchananalysis).Ultimately,theindivid-
ualbenefits conferredbydocks suggest thattheylikelyhave a positive
impacton the population of A. pisonii in the saltmarsh.Therefore, this
studysuggeststhatanthropogenichabitatshavethepotentialtoplayan
importantroleinprovidingimprovedconditionstorange-shiftingspecies
experiencing suboptimal conditions in colonizedecosystems. While no
habitatanalogislikelytoameliorateallnegativenovelinteractionsexpe-
riencedbyrange-shifting species, amelioration of evena small number
ofnegativeimpactswilllikelybe beneficialto bothindividuals andpop-
ulations.Ifthepatterns that we document are general across systems,
thenanthropogenichabitatsmayplayanimportantfacilitativeroleinthe
rangeshiftsofspecieswithcontinuedclimatechange.
ACKNOWLEDGMENTS
The authors thank K. Plumb and L. Carpenter for help with dissec-
tionsaswellasD.WetheyforguidanceinusingthedatafromNARR.
Additionally,we thank I. C. Feller foradvice 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,foraid andassistanceduring this study.This work
wassupported by NSFgrantno.OCE-1129166.Thisis Smithsonian
MarineStationcontributionnumber1077.
AUTHOR CONTRIBUTIONS
ZJC and BDG conceived and designed the experiments. ZJC con-
ducted field work and behavioral observations. ZJC and SRD col-
laboratedondissections andthermal imageanalyses. ZJCperformed
statisticalanalyses.ZJCwrotethemanuscript.BDGprovidededitorial
adviceandguidancethroughouttheproject.
CONFLICT OF INTEREST
Nonedeclared.
ORCID
Zachary J. Cannizzo http://orcid.org/0000-0002-0814-7555
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How to cite this article:CannizzoZJ,RiverDixonS,Griffen
BD.Ananthropogenichabitatwithinasuboptimalcolonized
ecosystemprovidesimprovedconditionsforarange-shifting
species.Ecol Evol. 2018;00:1–13. https://doi.org/10.1002/
ece3.3739
... Due to the relatively low nutrient content, a greater volume of plant material is needed to meet the same metabolic requirements that can be met with a smaller volume of animal material (i.e., compensatory feeding), which results in a larger gut over time for more herbivorous individuals. Previous studies demonstrate that gut width is a reliable predictor of diet in individual crabs [18,19], as well as at the population level by comparing across sites with different levels of food availability [20][21][22]. ...
... Like H. sanguineus, A. pisonii has been described as an opportunistic omnivore, feeding on animal material preferentially when it is available, while plant material still makes up the bulk of its diet (Erickson et al., 2008). Finally, gut size is a reliable predictor of diets of individual crabs for both of these species [18][19][20][21][22]. ...
... This surprising result may potentially be explained by anatomical constraints that disproportionately affect crab species that are primarily herbivorous. We have previously demonstrated that residual gut size increases with percent herbivory in these species [18,20,21], but this relationship appears to break down at very high levels of herbivory (>60%) [35]. This may result from the limited space inside the carapace and the tradeoff in space use amongst the gut and other organs (gills, hepatopancreas, gonads, etc.). ...
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... Reconciliation ecology argues for preserving global biodiversity by sharing human-modified landscapes, like cities, with other species [2]. The primary way people currently practice reconciliation ecology and provide habitat for other species in our cities is through urban green spaces [3]. Green spaces are critical pieces of urban green infrastructure [4,5] that improve urban environmental quality and human health and reduce the burden on existing grey infrastructure, such as stormwater drains [6][7][8][9]. ...
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... Red king crabs (Paralithodes camtschaticus) were more abundant on experimental pile structures in Alaska than adjacent seafloor, possibly due to habitat provided by colonizing hydroids (Stevens et al. 2004). Similarly, docks in the southeast U.S. provided forage from attached fouling organisms growing on piles for mangrove tree crabs (Aratus pisonii) (Cannizzo et al. 2018). In Australia, subtidal epibiota diversity and abundance increased on piles relative to open water, and unshaded piles had similar communities as natural rocky habitat (Connell and Glasby 1999). ...
... While impacts of small docks on vegetation have been well studied, studies of dock shading impacts on fish and invertebrate communities to date are mostly limited to large structures (i.e., piers, marinas, and bridges) and results may not scale to smaller private structures (Able et al. 2013). For example, most studies of piers have found negative shading effects on fish and invertebrates (Able and Duffy-Anderson 2005) while a study of small docks in the southeast U.S. showed that decking shading provided a beneficial thermal refuge to mangrove tree crabs (Cannizzo et al. 2018). Previous studies of large commercial piers have shown a variety of impacts including alteration of fish migratory behavior, habitat use, community composition, and growth (Munsch et al. 2017). ...
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Small docks and floats are common in estuaries and coastal waters worldwide. These structures serve a role in coastal recreation by facilitating access to waterways. However, they can impact shoreline ecological function. While individual environmental impacts are generally minor, increasing dock proliferation and overlap with sensitive coastal resources can result in cumulative impacts that pose threats at the ecosystem level. Docks promote changes in habitat and aquatic communities through alteration of environmental conditions. Here, we review the potential environmental impacts of docks on estuarine and coastal flora and fauna and discuss best management practices (BMPs) to avoid or minimize such impacts with a focus on New England. We consider impacts in relation to the structural components of docks: the piles, decking, and floats. Impacts to salt marsh and submerged aquatic vegetation are a particular focus given the important ecosystem services these vegetated habitats provide and their vulnerability to dock-induced habitat alteration. Potential environmental impacts depend on structure size, design, and location, and can include both short-term (e.g., turbidity from pile installation) and long-term (e.g., salt marsh loss from chronic shading) effects. Such effects can be minimized through BMPs (e.g., construction outside sensitive time-of-year periods, designs to reduce shading). As BMPs tend to reduce rather than avoid environmental effects, cumulative impacts also need to be considered in the permitting process. We recommend that managers develop plans or bylaws that identify sensitive habitats where dock construction should be avoided as well as BMPs to make remaining dock proliferation less impactful.
... Fortunately, relatively short-term changes in diet patterns can be assessed using crab gut morphology. As with other crab species 44 , the cardiac stomach (hereafter "gut") of A. pisonii increases in size as diet quality decreases, presumably to enable sufficient energy/nutrient consumption on a lower quality diet 45 . Animal tissue represents a higher quality diet for A. pisonii 25 , and so crabs that consume more animal tissue, or other high nutrient food sources, generally have smaller guts 44 . ...
... Animal tissue represents a higher quality diet for A. pisonii 25 , and so crabs that consume more animal tissue, or other high nutrient food sources, generally have smaller guts 44 . Gut size changes over short time intervals reflecting diet changes that occur on the order of weeks 45 , and thus gut size can be used as a reliable indicator of overall changes in diet quality throughout the reproductive season in this species 24,43 . We therefore regressed gut width against carapace width and used the residual from this regression as the response variable in our analysis to assess diet quality. ...
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Two common strategies organisms use to finance reproduction are capital breeding (using energy stored prior to reproduction) and income breeding (using energy gathered during the reproductive period). Understanding which of these two strategies a species uses can help in predicting its population dynamics and how it will respond to environmental change. Brachyuran crabs have historically been considered capital breeders as a group, but recent evidence has challenged this assumption. Here, we focus on the mangrove tree crab, Aratus pisonii , and examine its breeding strategy on the Atlantic Florida coast. We collected crabs during and after their breeding season (March–October) and dissected them to discern how energy was stored and utilized for reproduction. We found patterns of reproduction and energy storage that are consistent with both the use of stored energy (capital) and energy acquired (income) during the breeding season. We also found that energy acquisition and storage patterns that supported reproduction were influenced by unequal tidal patterns associated with the syzygy tide inequality cycle. Contrary to previous assumptions for crabs, we suggest that species of crab that produce multiple clutches of eggs during long breeding seasons (many tropical and subtropical species) may commonly use income breeding strategies.
... Studies on multiple species demonstrate that gut size is a valid proxy for the diet composition and diet quality of individual crabs. For example, Cannizzo et al. (2018) showed that mangrove tree crabs Aratus pisonii that eat a higher-quality diet have smaller guts than those that eat a lower-quality diet. Griffen & Mosblack (2011) used field experiments to determine that Asian shore crabs -the same species exa mined in this study -that choose to eat a higher-quality diet have smaller guts. ...
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Invasive species alter invaded ecosystems via direct impacts such as consumption. In turn, an invasive species’ ability to thrive in new habitats depends on its ability to exploit available resources, which may change over time and space. Diet quality and quantity are indicators of a consumer’s consumptive effects and can be strongly influenced by season and latitude. We examined the effects of season and latitude on the diet quality and quantity of the invasive Asian shore crab Hemigrapsus sanguineus throughout a non-winter sampling year at 5 different sites spanning 8° of latitude across its invaded United States range. We found that diet quality, averaged through time, largely follows an expected latitudinal cline, being higher in the center of its range and lower toward the southern and northern edges. We also found that while some sites show similar patterns of diet quality variation with season, no pattern is consistent across all latitudes. Finally, we found that crabs at sites with low diet quality during summer reproductive months did not compensate by increasing total consumption. Because the Asian shore crab is an important consumer in its invaded ecosystems, understanding how its diet quality and quantity vary with season and latitude can help us better understand how this species influences trophic interactions and community structure, how it has been able to establish across a wide ecological and environmental range, and where future range expansion is most likely to occur.
... Sin embargo, también es importante considerar que el cambio en el patrón de distribución en una especie en particular debida al CC, no se restringa solo al efecto en esa especie, ya que puede esperarse que esto tenga diferentes consecuencias en la estructura y funcionamiento en las comunidades en las que se encuentre o a las que se vaya introduciendo. La importancia de las consecuencias del cambio en la distribución de las especies por el CC dependerá fuertemente del papel que jueguen dichas especies dentro de la comunidad (Cannizzo et al., 2017;Castellanos et al., 2009;Schweiger y Settle, 2008). Es decir que la importancia relativa del cambio en el patrón de distribución de una u otra especie no será necesariamente equivalente y dependerá del efecto que cada una tenga en la funcionalidad de la comunidad (Bergin y Kimberley, 1997;Martínez et al., 2014;Reckendorf et al., 1985). ...
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Many animals have flexible morphological traits that allow them to succeed in differing circumstances with differing diets available to them. For brachyuran crabs, claw height and gut size are diet-specific and largely reflect foraging strategies, while abdomen width reflects relative levels of fecundity. However, the link between claw size and diet has largely been documented only for primarily carnivorous crabs, while the link between diet and fecundity is strong in herbivorous crabs. We sought to determine the nature of the intraspecific relationship between claw size, dietary habits, and fecundity for two primarily herbivorous crab species, Hemigrapsus sanguineus and Aratus pisonii . Specifically, we examined whether claw size and/or abdomen width can be used as reliable measures of individual diet strategy. To test these hypotheses, we collected crabs and measured the dimensions of their claws, abdomens, and guts. By comparing these dimensions for each individual, we found that strongly predictive relationships do not exist between these traits for the primarily herbivorous species in our study. Thus, identifying external morphological features that can be used to assess diets of primarily herbivorous crabs remains elusive.
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