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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.    
An anthropogenic habitat within a suboptimal colonized
ecosystem provides improved conditions for a range- shifting
Zachary J. Cannizzo1| Sara R. Dixon1| Blaine D. Griffen2
©2018TheAuthors.Ecology and EvolutionpublishedbyJohnWiley&SonsLtd.
Funding information
Manyspeciesareshifting their ranges in response to the changing climate. In cases
speciesmay play acrucial role inthe ability ofthat species toexpand or persistin
treecrabAratus pisoniiwithinthecolonizedsuboptimalsaltmarshecosystem.Totest
aging,andthethermalconditionsof A. pisonii in each habitat. We found that docks
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
Aratus pisonii,climatechange,habitatanalog,mangrove,saltmarsh,thermalhabitat
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
foundation species (Walther, 2010). However, differential shifting
whichithasneverpreviouslyinhabited (Schweiger,Settle,& Kudrna,
   CANNIZZO et Al.
ratesisexpectedtoincreaseas climatechangecontinues(Schweiger
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,
how these shifts impact the species themselves.This is particularly
true of rangeshifts which result in the colonization of new ecosys-
ronmentalinteractions. Due to the complexity of these interactions,
predicting how theywill impact both the colonized ecosystem and
abundantresearchonthe impact ofnovel species oncolonizedeco-
& 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
systemthat differs greatlyfromitshistoricecosystemin foundation
species(Holt,Barfield,& Gomulkiewicz,2005;Keller&Taylor,2008).
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,
Despitethedifficulties faced byacolonizingspecies, pocketsof
mayexist within the colonized ecosystem. Thesepockets of habitat
habitat” from the urban and reconciliationecology literature (sensu
Lundholm& Richardson,2010).Habitatanalogs havereceivedsome
urbanrubble (Grant, 2006) and oftenprovidehabitat and refugefor
(Chester&Robson,2013;Lundholm& Richardson,2010). Whilethe
the historic ecosystem ofthe colonizer. Whether naturalor anthro-
pogenic,analogoushabitatsand otherrefugesmayprovide benefits
Smart,Wilson, & Maclean,2016;Wilsonetal., 2015), predation ref-
uge (Dumont, Harris, & Gaymer,2011), and higher quality foraging.
shifts.However,theimpactofanalogous habitats and other refuges
ThemangrovetreecrabAratus pisoniioffersanideal opportunity
toexamine the impacts ofboth a colonizedecosystemand a poten-
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,&
alterniflora,differsgreatlyfromthe mangroveforestswhereA. pisonii
hashistoricallybeen found.Themangroveprovidesashadedhabitat
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-
for A. pisonii. However,A. pisonii is alsofoundon the anthropogenic
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-
ispreferredbyA. pisoniiovermangroveleaves(Erickson, Feller,Paul,
couldbe a boon to A. pisonii as the quantity and quality ofdiet play
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
lifehistory(Huey,1991;Leffler,1972), especiallywhenwarmerthan
optimal(Gillooly,Brown,West, Savage,&Charnov,2001). Thus, the
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,
&Zavaleta,2009). However,these structures havealwaysbeende-
in a colonized natural ecosystemthat was not intended to improve
logicalandlifehistorytraitsofA. pisoniithatinfluencebothindividual
thesaltmarsh.This includes aspects of behaviorrelatedto diet and
energystorage, thermal conditionsexperiencedbyA. pisonii, andan
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
2.1 | Study species
Aratus pisonii is a mangrove-associated crab found throughout the
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
grove leaves, specifically from the red mangrove R. mangle (Beever
etal., 1979; López & Conde, 2013). Individuals maintain strong site
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,
black(Avicennia germinans)andred
(Rhizophora mangle)mangroves(Williams,
   CANNIZZO et Al.
andeven exhibitsa characteristic climbingbehavior to avoidaquatic
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
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
redmangrove, the species to which theecologyofA. pisoniiis most
&Griffen, 2016). Further, evenifthere is some movement between
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
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
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
into holes, release in the salt marsh occurred during the rising tide
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-
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,
binocularsto avoidimpacting theirbehaviorand monitoredthe indi-
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
Weseparated the observations into ebb and flood tidal periods
to examine differences in foragingbehavior as crabs gained or lost
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
To test for the effects of multiple biological and environmental
Behavior Description
Feeding Thecrabisobservedactivelymovingitsclawsfromafooditemorsubstratetoits
Moving Thecrabisactivelymovingalongasubstrateandnotfeeding.Otherenergy-
Sitting Thecrabisnotactivelymoving,feeding,orparticipatinginanyactivity
TABLE1 Ethogramdescribingthe
observingAratus pisonii
tribution.We included carapacewidth,sex,habitat,airtemperature,
andtide(ebborflood) asexplanatoryvariables.Wealsoincludedthe
bythe total time ofobservation for eachindividual.Additionally,we
exploredtheproportionoftimeA. pisoniispentmovingbyemployinga
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-
weplacedHOBO thermal data loggers underneath a dock, and in a
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
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
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-
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
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
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-
(~6hrdependingonsite andday)wouldimpacttheirbodytempera-
solarradiationatthe gridpointclosesttoeachsiteand averagedthe
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
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
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,
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-
portionof timeindividualsspent in thewaterand sunaswell asthe
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
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
   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
kept frozen until dissection. No measured indices differed between
Based on preliminary observations in the laboratory, the gut
clearancetime ofA. pisonii is ~3hr.Therefore,our collection regime
(collectedon the flood tide), when crabs only had access to unsub-
mergedhabitat(collectedatslack hightide),andwhen crabshadac-
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
(212)×Gut width3
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
timeofcollection (seebelow),onlygutfullnesswasimpactedbythis
measuring the cardiac stomach ofeach crab to the nearest 0.1mm
andcomparingthe gut-width:carapace-widthratio betweenhabitats.
ratiocorresponding toahigherquality dietthatlikelycontainsmore
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
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
crabsas male, gravid female, or nongravid female and comparedthe
obtainaweight for somatic tissue from these 10 crabs resulting in a
2.6 | Statement of animal rights
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
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,
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.
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-
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,
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
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
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-
z=−1.73p=.084).Theinteraction betweenmovement andtidere-
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
differbetweenthemangroveand saltmarsh(GLM, estim.=−2.433,
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
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
FIGURE3 (a)Boxplotscomparingtheproportionoftimespent
insunbyAratus pisoniibetweenthethreehabitats.Groupsthatare
   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
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
p<.001), as solar exposure increased (LMER, estim.=−0.4262,
t105=−2.23p=.02813), and as crabs spent more time in thewater
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;
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,
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-
suggeststhat gutfullnesswas dependentona combinationofthese
variables.Whenanalyzedbyhabitat,itisclearthatA. pisoniiwereable
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
FIGURE5 BoxplotsshowingthegutfullnessofAratus pisoniiby
gut-width:carapace-width ratio, indicating a lower quality long-term
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
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-
Compared to the historic mangrove, the salt marsh proved to be a
suboptimal habitat for A. pisonii in every measured aspect of this
providingimproved conditionsforA. pisonii within thecolonizedsalt
Oneimportant benefitconferredby docks islargerbody size. While
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
Understanding how analogous habitats confer general benefits,
oftheprecisewaysinwhich ananalogoushabitatprovidesimproved
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,
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
tofood,docksprovideabundantanimalprotein,ahigh-quality food
nities.We regularlyobservedA. pisoniifeedingonfoulingorganisms
suggesting that animal material plays an important role in the im-
FIGURE6 Boxplotscomparingthegut-width:carapace-width
ratiosofAratus pisoniibetweenthemangrove,saltmarsh,anddock
FIGURE7 Boxplotscomparingtheinvestmentinlong-term
female,andnongravidfemaleAratus pisoniibetweenthethree
   CANNIZZO et Al.
leadto otherbenefitsincluding largersize(Huey,1991; Leffler,1972).
ForA. pisonii,docksprovideashadedthermalrefugewhichallowscrabs
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
providecrabsa coolerhabitat duringsummer months,the abilityofan
analogoushabitattoprovidea warmer microhabitat in winter months
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-
ulatebydipping inwatertocoolthemselvesafterextendedtimein the
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
via evaporative cooling(Eshky, Atkinson, & Taylor, 1995), which could
posuretothesunsurelyhasanacutewarmingimpact oncrabs, itssta-
The change in thermoregulatorybehavior in the salt marsh sug-
conditions in colonized ecosystems:by allowing individuals to avoid
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
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
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
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
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
to minimize the exposure ofvulnerable species to stressful changing
sprinklers foramphibians (Shoo etal., 2011), artificial breeding struc-
habitat restoration using artificial structuressuch as burrows (Souter
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).
otherunfavorablehabitats to encouragethe movementofspecies be-
species to persist in the face of changing climatic conditions(Krosby
etal., 2010; Williams, Eastman etal., 2014;Williams, Lundholm etal.,
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,
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
Asclimate changecontinuesto forceor encouragespecies to colo-
ashabitatanalogsmayplayacrucialroleinthe outcomeofrangeshifts.
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
experiencing suboptimal conditions in colonizedecosystems. While no
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,
The authors thank K. Plumb and L. Carpenter for help with dissec-
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
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
Zachary J. Cannizzo
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... 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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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.
... 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]. ...
... As climate change progresses, the negative impacts of sea-level rise, floods, drought, and extreme temperatures will degrade and reduce the habitat urban green spaces provide; thereby, reducing the biodiversity they sustain [22]. Addressing climate change through the lens of reconciliation ecology means ensuring a supply of habitat during times of stress so that species are not forced to shift their natural ranges and occupy novel geographic areas [3]. A study conducted by Berdejo-Espinola et al. [35] demonstrated the importance of accessible green spaces for humans to engage in nature-based coping mechanisms during times of stress. ...
... In addition to absorbing and slowing surface water runoff, green roofs can provide habitat redundancy during flood events, providing species with opportunities to retreat from the unfavorable conditions in other ground-level habitats [61]. Green roofs and other habitat installations, such as artificial or modified shading, humidifying, and sheltering structures, as well as those suitable to support breeding in target species, can be important tools to help humans and non-human species adapt to climate change impacts in urban environments by providing microhabitat refuges and reducing stress [3,93]. The process for mapping flooding impacts on existing green space conducted in this study is one way to identify which species or ecosystem services need to be prioritized in key locations. ...
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The practice of reconciliation ecology in urban environments relies heavily on urban green space as the primary source of vegetated habitat in cities. However, most cities lack the quantity, connectivity, and accessibility of green space needed to provide essential ecosystem services for the health, well-being, and resilience of human and non-human species. In reaction to urban densification and the increasing frequency and severity of climate change impacts, this study argues that architecture could strategically provide vegetated habitats to supplement existing urban green space and provide refuges for non-human species during extreme disturbances. A spatial analysis was conducted to test the performance of the existing green space network against targets for human well-being and Indigenous avifauna habitat needs in a 1.93 km2 neighborhood in Wellington, Aotearoa New Zealand, during normal conditions and flooding. The results showed an insufficient quantity and connectivity of green space during both normal conditions and flooding to meet the habitat needs of Indigenous avifauna. Though the per capita green space and accessibility targets for human well-being are met under normal conditions, there is insufficient green space to meet those targets during flooding. During normal conditions, 9% of the roofs in the neighborhood need to be converted to green roofs to achieve the targets for both human well-being and Indigenous avifauna. The amount increases to 17% if the targets are to be maintained during flooding. At least 3% of the roofs need to function as small and medium-sized habitat patches in key locations to increase the existing green space network's connectivity. The study concludes that though ground-level green space is limited, with regenerative architecture strategies and supporting governance policy, the surplus of existing roofs could be used to increase urban habitat provision, thereby enhancing the health and resilience of humans and Indigenous avifauna in cities.
... 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). ...
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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The consequences of climate change on ecosystems may depend largely on their effect on the distribution of species that play a key role in communities. The aim of this work was to model the potential distribution, current and future, of 5 key species of coastal dune vegetation of the Yucatán Peninsula. Particularly the expected changes in areas currently destined for conservation were evaluated. The maximum entropy method was used, including the RCP 4.5 and 8.5 scenarios, which respectively consider a moderate and drastic increase in greenhouse gas emissions, and the general CNRM-CM5 circulation model to the 2080 horizon. The models showed that under both scenarios, the distribution of the selected species would decrease markedly, with a reduction from 72% to 94% for scenario 4.5 and from 82% to 93% for scenario 8.5, and that most of the protected natural areas would not maintain favorable environmental conditions for the 5 species studied. However, it was identified that protected areas northeast of the peninsula, and an unprotected area at the north of the state of Yucatán, could conserve a limited area that would favor the distribution of these species.
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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.
Full-text available
Climate change is transforming ecosystems and affecting ecosystem goods and services. Along the Gulf of Mexico and Atlantic coasts of the southeastern United States, the frequency and intensity of extreme freeze events greatly influences whether coastal wetlands are dominated by freeze‐sensitive woody plants (mangrove forests) or freeze‐tolerant grass‐like plants (salt marshes). In response to warming winters, mangroves have been expanding and displacing salt marshes at varying degrees of severity in parts of north Florida, Louisiana, and Texas. As winter warming accelerates, mangrove range expansion is expected to increasingly modify wetland ecosystem structure and function. Because there are differences in the ecological and societal benefits that salt marshes and mangroves provide, coastal environmental managers are challenged to anticipate effects of mangrove expansion on critical wetland ecosystem services, including those related to carbon sequestration, wildlife habitat, storm protection, erosion reduction, water purification, fisheries support, and recreation. Mangrove range expansion may also affect wetland stability in the face of extreme climatic events and rising sea levels. Here, we review current understanding of the effects of mangrove range expansion and displacement of salt marshes on wetland ecosystem services in the southeastern United States. We also identify critical knowledge gaps and emerging research needs regarding the ecological and societal implications of salt marsh displacement by expanding mangrove forests. One consistent theme throughout our review is that there are ecological trade‐offs for consideration by coastal managers. Mangrove expansion and marsh displacement can produce beneficial changes in some ecosystem services, while simultaneously producing detrimental changes in other services. Thus, there can be local‐scale differences in perceptions of the impacts of mangrove expansion into salt marshes. For very specific local reasons, some individuals may see mangrove expansion as a positive change to be embraced, while others may see mangrove expansion as a negative change to be constrained.
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Pomacea canaliculata is a freshwater snail native to southern South America. The aims of this work are to update its distribution in Argentina and to analyze through niche models whether the environmental conditions from its original distribution can anticipate its recently expanded range. Almost all records of P. canaliculata before 1958 (original records) belong to del Plata or connected basins. A quarter of the new present records are located in basins not connected to del Plata, indicating a recent expansion of the distribution range of P. canaliculata in Argentina. Recently colonized areas are mostly environmentally suitable according to the projection of the original distribution model, thus natural barriers were probably the main limits to its distribution in the past. According to the model, many regions outside its original range, including several not yet colonized, are suitable for the establishment of P. canaliculata. Consequently, it is likely that this species will continue establishing new populations in Argentina, especially if fishermen and aquarists continue to move snails to new locations. Our study revealed that an extensive but overlooked invasion is in process in its native range, where the impacts on diversity and ecosystems functioning may differ from those already described elsewhere.
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Nonlethal injury is a common and ubiquitous feature of marine systems and can result in altered growth and survival rates. Ecological theory predicts that injured animals should face an energetic tradeoff between investing in recovery vs. investing in reproduction. Possible impacts on reproduction may range in magnitude from very strong (elimination of reproduction), to intermediate (reduced number of offspring), to weak (reduced investment in each offspring). While this tradeoff is well established in terrestrial systems, it has received little attention in the marine environment, particularly in a way that quantitatively relates the degree of injury to the degree of reproductive impact. We examined injury via limb loss across 4 sites in the mangrove tree crab Aratus pisonii . We found that limb loss was highest at the site that was closest to roads and had the highest level of human presence, and conversely, injury was lowest at the site furthest from the road and with the lowest level of human presence. We found evidence that the quality of consumed food likely decreases with the number of limbs lost, but found no influence of limb loss on amount of food consumed or on energy storage. We show that limb loss reduced the number of eggs produced and that the mass of the ovary declined with the number of regenerating limbs, providing direct evidence for a tradeoff between reproduction and injury recovery. Further, our study therefore suggests that these impacts may increase with the level of human disturbance.
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Range shifts and expansions resulting from global climate change have the potential to create novel communities with unique plant-animal interactions. Organisms expanding their range into novel biotic and abiotic environments may encounter selection pressures that alter traditional biogeographic patterns of life history traits. Here, we used field surveys to examine latitudinal patterns of life history traits in a broadly distributed ectotherm (mangrove tree crab Aratus pisonii) that has recently experienced a climate change-induced range expansion into a novel habitat type. Additionally, we conducted laboratory and field experiments to investigate characteristics associated with these life history traits (e.g. fecundity, offspring quality, and potential selection pressures). We compared these characteristics in native mangrove habitats in which the species has historically dwelled and novel salt marsh habitats into which the species has recently expanded its range. Consistent with traditional biogeographic concepts (i.e. Bergmann's clines), size at maturity and mean body size of reproductive females increased with latitude within the native habitat. However, they decreased significantly in novel habitats at the highest latitudes of the species' range, which was consistent with habitat-specific differences in both biotic (predation) and abiotic (temperature) selection pressures. Although initial maternal investment (egg volume and weight) did not differ between habitats, fecundity was lower in novel habitats as a result of differences in size at reproduction. Offspring quality, as measured by larval starvation resistance, was likewise diminished in novel habitats relative to native habitats. These differences in offspring quality may have enduring consequences for species success and persistence in novel habitats. Life history characteristics such as those investigated here are fundamental organismal traits; consequently, understanding the potential impacts of climate change responses on latitudinal patterns of these traits is key to understanding climate change impacts on natural systems. © 2017 Riley, Griffen. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Reproduction is energetically financed using strategies that fall along a continuum from animals that rely on stored energy acquired prior to reproduction (i.e., capital breeders) to those that rely on energy acquired during reproduction (i.e., income breeders). Energy storage incurs a metabolic cost. However, previous studies suggest that this cost may be minimal for small-bodied ectotherms. Here I test this assumption. I use a laboratory feeding experiment with the European green crab Carcinus maenas to establish individuals with different amounts of energy storage. I then demonstrate that differences in energy storage account for 26% of the variation in basal metabolic costs. The magnitudes of these costs for any individual crab vary through time depending on the amount of energy it has stored, as well as on temperature-dependent metabolism. I use previously established relationships between temperature- and mass-dependent metabolic rates, combined with a feasible annual pattern of energy storage in the Gulf of Maine and annual sea surface temperature patterns in this region, to estimate potential annual metabolic costs expected for mature female green crabs. Results indicate that energy storage should incur an ~8% increase in metabolic costs for female crabs, relative to a hypothetical crab that did not store any energy. Translated into feeding, for a medium-sized mature female (45 mm carapace width), this requires the consumption of an additional ~156 mussels annually to support the metabolic cost of energy storage. These results indicate, contrary to previous assumptions, that the cost of energy storage for small-bodied ectotherms may represent a considerable portion of their basic operating energy budget. An inability to meet these additional costs of energy storage may help explain the recent decline of green crabs in the Gulf of Maine where reduced prey availability and increased consumer competition have combined to hamper green crab foraging success in recent years.
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General circulation models predict warming trends and changes in temperature and precipitation patterns that have the potential to alter the structure and function of coastal habitats. The purpose of this study was to quantify the expansion and contraction of mangroves and saltmarsh habitats and assess the impact of climate on these landscape changes. The study was conducted in a mangrove/saltmarsh ecotone in Flagler County, FL, near the northern range limit of mangroves along the Atlantic coast of North America. We used time series of historical aerial photography and high-resolution multispectral satellite imagery from 1942 to 2013 to quantify changes in the extent of mangrove and saltmarsh vegetation and compared these changes to climate variables of temperature and precipitation, temperature–seasonality, as well as historical sea-level data. Results showed increases in mangrove extent of 89% between 1942 and 1952, and a continuous increase from 1995 to 2013. Largest decrease in saltmarsh extent occurred between 1942 and 1952 (-136%) and between 2008 and 2013 (-81%). We found significant effects of precipitation, temperature, seasonality, and time on mangrove and saltmarsh areal extent. The statistical effect of sea-level was rather small, but we speculate that it might have ecological impacts on these two coastal ecosystems. Results also showed a cyclical dynamism as well as a reversal in habitat dominance, which may be the result of complex interactions between plant habitats and several environmental drivers of change such as species interactions, and hydrological changes induced by sea-level rise, in addition to temperature and precipitation effects. Our results on mangrove/saltmarsh expansion and contraction may contribute to the improvement of management and conservation strategies for coastal ecosystems being impacted by climate change.
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As ecological communities migrate northward with climate change, associated species are expected to accompany habitat-forming, foundation species. However, differences in physiological limitations and/or sensitivity to climatic cues can cause spatial or temporal mismatches in the expansion of foundation species and associated inhabitants. Here, we document novel habitat switching by an inhabitant that has outpaced its traditional habitat. We provide the first report of the typically mangrove-associated Aratus pisonii (Mangrove Tree Crab) in temperate salt marsh habitats along Florida's Atlantic coast. Mangrove Tree Crab is present in salt marshes as far north as Little Satilla Creek, GA (31°5′32″N), substantially further north than the northernmost mangrove (∼30°N). Based on historical records of the range limit of Mangrove Tree Crab and its current distribution, we calculate that the species has moved northward at a rate of 62 km per decade over the last century, outpacing the range expansions of the foundation species (13–45 km/decade) with which it has traditionally been associated.
An emerging focus of behavioural ecology is to determine the driving forces behind animal personalities. While numerous theories have been proposed to explain these behavioural variations, empirical studies on this subject remain lacking. Here, we test ecological theory by studying the combined effects of physiological condition and habitat quality on the behaviour of individual mud crabs, Panopeus herbstii, across the spawning season (early spawning season and 2 months after). We assessed the boldness, energy stores and reproductive effort of crabs collected across 10 oyster reefs of low and high quality using laboratory observations and subsequent dissections. Crab boldness was significantly dependent on the interaction between habitat quality and season. While crab behaviour remained relatively constant on healthy reefs, crabs on degraded reefs exhibited a nearly two-fold increase in boldness during the late spawning season, approximating the boldness of crabs on healthy reefs. This behavioural change corresponds to a seasonal shift in crab energy store content and is likely to represent a switch in the primary driving force of crab behaviour. During the early season, crab boldness was positively correlated with short-term stores, whereas later in the season, crab boldness was negatively correlated with long-term stores. Our results suggest that behaviour is driven by predation pressure and refuge availability during the early spawning season, but afterwards depends on replenishing energy stores used for reproduction. These findings support ecological theory and also provide new insight into the stability of behavioural drivers.
Climate-mediated range shifts into eco-evolutionary novel habitats have the potential to alter the ecology and behaviour of range-expanding species. Of particular concern are behaviours that have a strong impact on the ecology and life history of expanding species. Behaviours that control the spatial patterns of habitat use may be particularly important. We examined site fidelity and foraging foray behaviour of the mangrove tree crab, Aratus pisonii, in its historic mangrove habitat and the recently colonized eco-evolutionary novel salt marsh. In the mangrove, A. pisonii showed both strong site fidelity to individual trees and a foraging pattern wherein they made foraging forays that decreased in frequency as their distance from the home tree increased; but they displayed neither behaviour in the salt marsh. Chemical cues from faeces appear to be the mechanism behind site fidelity in the mangrove and may suggest the mechanism for the loss of this behaviour in the salt marsh where substrate is regularly submerged, potentially preventing establishment of such cues. The loss of site fidelity may affect the foraging behaviour and predation risk of A. pisonii in the salt marsh, leading to a shift in its ecology and bioenergetics. As more species are forced to shift ranges into eco-evolutionary novel habitats, it is important to understand how this shift may affect their life history, behaviour and ecology in indirect ways.
Thermal biology of lizards affects their overall physiological performance. Thus, it is crucial to study how abiotic constraints influence thermoregulation. We studied the effect of wind speed on thermoregulation in an endangered mountain lizard (Iberolacerta aurelioi). We compared two populations of lizards: one living in a sheltered rocky area and the other living in a mountain ridge, exposed to strong winds. The preferred temperature range of I. aurelioi, which reflects thermal physiology, was similar in both areas, and it was typical of a cold specialist. Although the thermal physiology of lizards and the structure of the habitat were similar, the higher wind speed in the exposed population was correlated with a significant decrease in the effectiveness thermoregulation, dropping from 0.83 to 0.74. Our results suggest that wind reduces body temperatures in two ways: via direct convective cooling of the animal and via convective cooling of the substrate, which causes conductive cooling of the animal. The detrimental effect of wind on thermoregulatory effectiveness is surprising, since lizards are expected to thermoregulate more effectively in more challenging habitats. However, wind speed would affect the costs and benefits of thermoregulation in more complex ways than just the cooling of animals and their habitats. For example, it may reduce the daily activity, increase desiccation, or complicate the hunting of prey. Finally, our results imply that wind should also be considered when developing conservation strategies for threatened ectotherms.
The cultivation of grapevines for winemaking, known as viticulture, is widely cited as a climate-sensitive agricultural system that has been used as an indicator of both historic and contemporary climate change. Numerous studies have questioned the viability of major viticulture regions under future climate projections. We review the methods used to study the impacts of climate change on viticulture in the light of what is known about the effects of climate and weather on the yields and quality of vineyard harvests. Many potential impacts of climate change on viticulture, particularly those associated with a change in climate variability or seasonal weather patterns, are rarely captured. Key biophysical characteristics of viticulture are often unaccounted for, including the variability of grapevine phenology and the exploitation of microclimatic niches that permit successful cultivation under sub-optimal macroclimatic conditions. We consider how these same biophysical characteristics permit a variety of strategies by which viticulture can adapt to changing climatic conditions. The ability to realise these strategies, however, is affected by uneven exposure to risks across the winemaking sector, and the evolving capacity for decision-making within and across organizational boundaries. The role grape provenance plays in shaping perceptions of wine value and quality, illustrates how conflicts of interest influence decisions about adaptive strategies within the industry. We conclude by considering what lessons can be taken from viticulture for studies of climate change impacts and the capacity for adaptation in other agricultural and natural systems. This article is protected by copyright. All rights reserved.