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Natural Areas Journal 30:�–19
Responses of Rare Plant Species to Fire in Florida’s Pyrogenic
Communities
Jodi L. Slapcinsky1,3
Doria R. Gordon1
Eric S. Menges2
1TheNatureConservancyandDepartmentofBiology
P.O.Box118526UniversityofFlorida,Gainesville,FL
32611
2ArchboldBiologicalStation
P.O.Box2057LakePlacid,Florida33862
3Correspondingauthor:jslapcinsky@tnc.org
� Natural Areas Journal Volume 30 (1), 2010
Natural Areas Journal 30:�–19
•
Responses of Rare Plant Species to Fire in Florida’s Pyrogenic
Communities
Jodi L. Slapcinsky1,3
Doria R. Gordon1
Eric S. Menges2
1TheNatureConservancyandDepartmentofBiology
P.O.Box118526UniversityofFlorida,Gainesville,FL
32611
2ArchboldBiologicalStation
P.O.Box2057LakePlacid,Florida33862
•
R E S E A R C H A R T I C L E
3Correspondingauthor:jslapcinsky@tnc.org
ABSTRACT:Lightning-andhuman-ignitedfireshaveshapedmanyofFlorida’snaturalcommunities.Plantpersistenceinthesehabitatsrequiresadaptationtosurvivehightemperatures,abilitytorespondtoabovegroundtissueloss,oravoidanceoftheseconditionsthroughsurvivalinunburnedpatchesorinthesoilseedbank.Limiteddistributionofmanyrarespecies in increasinglyfragmentedhabitatsanduncertaintyofwhetherrarespeciestolerate,require,orpersistthroughavoidanceoffirehampersfiremanagementwhenitispossibleandthreatenslong-termviabilityofplants.Wereviewupto14yearsofmonitoringdatafor18rareplantspeciesfrom14familiesoccurringonsandhill,scrub,pinerock-land,andmixeddeciduoushardwoodcommunitiesacrossFlorida.Foranumberofvariablesmeasured,includingdensity,frequency,flowering,andrecruitment,50%ofthespeciesshowedsignificantpositiveresponsestoburningand50%ofthespeciesshowedaneutralornoresponse.Noneofthespecieswereunabletorecoverpost-burn.Theseresultssuggestthatprescribedfireinthesepyrogenichabitatsneednotbedelayeduntilspecies-specificresponsestofireareunderstood.
Index terms:fire,Florida,Floridascrub,pinerocklands,pyrogenic,sandhill
INTRODUCTION
Recenthypothesessuggestthatfireplaysanimportantroleinshapingthecharacteristicsofmanyoftheworld’sbiomes(BondandKeeley2005).Fire-adaptedorpyrogenicecosystemshavebeenestimatedtocover40%oftheworld’slandsurface(Chapinetal2002),andit is thefireregime(fireintensity,severity,frequency,andseason)thathascreatedsomeofthemostbiodiversehabitats. Fire-adapted habitats includetropicalsystemsthatburninthedryseason,likesavannawoodlands,monsoonforestsandtropicalpineforests(Nasietal.2002),MediterraneanclimateregionsoftheworldthatincludehabitatsoftheMediterraneanbasin,Californiachaparral,SouthAfricanfynbosandAustralianheathlands(Cowl-ingetal.1996;BondandKeeley2005),andcircumpolarborealforests,taigaandtundra habitats with permafrost (Nasi etal.2002).
Among North American fire-maintainedecosystems are grasslands, prairies, andpineforeststhatrepresentover90%ofthesoutheastern United States (Frost 1995).Thesesystemsaresubstantiallyinfluencedbylightning-andhuman-ignitedfireandtropical storms (Brockway and Lewis1997).PeninsularFloridahasoneof thehighest incidencesof lightningstrikes intheworld(GoodmanandChristian1993).Lightningflashdensitiesaregreaterthan30flkm-2yr-1,secondonlytotheworld“hotspot” in the equatorial Congo Basin(Christianetal.2003).Historically,mostfireswerecausedbylightning,whichwasmostprevalentduringtheconvectivestormevents of the growing season (Huffman
2006).Pastfireregimeswereaugmentedby nativeAmerican-ignited fires (Brown2004) often set during times other thanthe lightning fire season (Snyder 1991).Today, prescribed fire for conservationand agricultural purposes now generallyreplacesthesenaturalandhistoricsourcesoffires(RobbinsandMyers1992).
As a consequence of fire’s consistentpresence on the Florida landscape, ap-proximately70%percentoftheterrestrialnaturalplantcommunitiesandnearly100%ofthepalustrinenaturalplantcommunitiesdescribed by the Florida Natural AreasInventory(1990)areconsideredfire-depen-dentorfire-adapted.Bothwide-rangingandgeographicallyrestrictedspeciesinthesecommunities have developed life historystrategiesinresponsetofire(MengesandKohfeldt1995).
Yearsoffire-suppressionandlossofhabitatdue to landdevelopment and conversion(Brockway andLewis1997)have led todeclining distributions of Florida’s rarespecies,especiallyinFloridascrub(Halletal.2002),pinerocklands(U.S.FishandWildlifeService1999),andsandhill(Noss1989;Frost1993).Landmanagersareoftenreluctanttousefireasamanagementtoolunless there are assurances that fire willnotthreatenimperiledspecies.Firereturnintervals,identifiedasthenumberofyearsbetween two successive fire events at aspecificsite,arecurrentlyincreasingevenwherefiremanagementdoesoccur(Hardin2002;Mulhollandetal.2003).In1926,theFloridaDepartmentofForestryandParksestimatedthatroughly5,260,921hectares,orapproximately75%ofthepinelandsin
Volume 30 (1), 2010 Natural Areas Journal �
Florida, burned annually (Baker 1926).From 1995 to 2003, the average annualnumberofhectaresthatburnedinFloridawasestimated tobe76,486,or less than1%ofthestate(FloridaDivisionofFor-estry2005).
GiventheimportanceoffiretorarespeciesinuplandFloridaecosystems,andthelikelynegativeimpactsoffiresuppression,moreinformationonfireresponsesofFlorida’srareplantsisessential.Here,weintegratepost-burndataonrarespeciesabundancesand vital rates (e.g., survivorship andreproduction),focusingondatacollectedby The Nature Conservancy (TNC) andArchboldBiologicalStation(ABS).Overthepast15years,bothorganizationshaveimplementedmonitoringandmanagementprogramsoftherareplantspeciesthatoccurontheir,andsomepubliclyowned,proper-ties.Theplantspeciesinbothmonitoringprogramsareglobally(rankedG1-G3)andlocally rare.NearlyeverynaturaluplandcommunitymaintainedbyfireinFloridaisrepresentedwithinthesepreservesandbothorganizationsmanagetheirpropertieswithfire(amongothermethods)atfrequenciesdependingonvegetationtype(RobbinsandMyers1992).Wesummarizetheresponsesof18rareplantstofire.
METHODS
Populationsof15ofthe18rareplantspe-cieshavebeenmonitoredannuallyon10preservespreviouslyorcurrentlyownedbyTNCinFlorida(Figure1).TheremainingthreespeciesweremonitoredonpropertyownedandmanagedbyABSormonitoredbyABSonpublicconservationareas.Allspeciesaremonitoredonhabitatsthatburnperiodicallyeithernaturallybylightning-causedfiresorbyprescribedfireathypoth-esizednaturalintervals(Table1).
Six of the rare species are found in oneof more than seven types of scrub habi-tats (e.g., scrubby flatwoods, white sandscrub, oak scrub; seeAbrahamson et al,1984,Menges1999,andSchmalzer2003for descriptions) on the preserves wherethey were monitored (Figure 1). For thepurposes of this paper, “Florida scrub”will be used for all Florida scrub-types.ThishabitatisfoundonABS(Highlands
County)andSaddleBlanketScrubPreserve(PolkCounty)locatedontheLakeWalesRidge (LWR). This relict shoreline anddunesystemischaracterizedbyrelativelyhigh elevation and excessively drainingsandysoils,anddatesbacktoatleastthePleistocene (White 1970; Myers 1990;Webb1990).Floridascrubismaintainedby recurrent disturbances including fire(Myers1990;GibsonandMenges1994;Menges1999) at intervals of every8-16years for scrubby flatwoods, every 5-12years for oak-hickory scrub, and every15-30yearsforrosemaryscrub(Menges2007). For our purposes, we define thefire return interval as a range from 5-30years(Table1).
Six species were monitored in sandhillat Tiger Creek Preserve (Polk County),CrookedLakeSandhillPreserve(VolusiaCounty),RockHillPreserve(WashingtonCounty),ApalachicolaBluffsandRavines
Preserve(LibertyCounty),andABS(Table1). InFlorida, longleafpine systemsoc-curmostly in thenorthandcentralpartsof the state, on gently rolling terrain ondeep,excessivelydrained,mostlyyellow,oligotrophic sands. These systems arecharacterized by frequent, low intensitylightning-causedfires thatoccurwithre-turnintervalsofonetofiveyears(Table1)(Christensen1981;MeansandGrow1985;Noss1989;Glitzensteinetal.1995).
Threeofthesixspeciesthatweremonitoredin scrubwerealsomonitored in sandhillhabitats(Table1).Bonamia grandiflora(A.Gray)Hallierf.wasmonitoredinsandhillatbothSaddleBlanketScrubPreserveandTiger Creek Preserve. Eriogonum longi-foliumNutt.var.gnaphalifoliumGandog.wasmonitoredinbothscrubandsandhillatArchboldBiologicalStation,andCon-radina brevifoliaShinnerswasmonitoredonbothhabitatsatSaddleBlanketScrub
Figure 1. Ten preserves, their associated habitat(s) and 18 species monitored in Florida.
� Natural Areas Journal Volume 30 (1), 2010
Spec
ies
Mon
itore
dha
bita
t(s)
Hab
itat f
ire
inte
rval
(yea
rs)
Var
iabl
e(s)
# Po
p#
BU
# SU
SU si
zeY
ears
pre
- an d
post
-bur
nan
alyz
ed
Bige
low
ia n
utta
llii
sand
hill
1-5a
% fl
ower
ing,
dens
it y1
720
30 x
1 m
0, 2
, 4, 6
Bona
mia
gra
ndifl
ora
sand
hill,
Flo
rida
scru
b1-
5a , 5-3
0bto
tal d
ensi
ty,
recr
uit d
ensi
ty,
%re
prod
uctio
n2
4-
-1-
10, 2
1-25
Cha
mae
cris
ta li
neat
a v
ar.
keye
nsis
pine
rock
land
2-15
cde
nsity
12
2650
x 2
m0-
6
Cha
mae
syce
del
toid
ea
subs
p. se
rpyl
lum
pine
rock
land
2-15
cfr
eque
ncy
12
2150
x 2
m0-
6
Con
radi
na b
revi
folia
sand
hill,
Flo
rida
scru
b1-
5a , 5-3
0bde
nsity
12
361
x 2
m0-
5
Con
radi
na g
labr
asa
ndhi
ll1-
5ade
nsity
12
793
x 3
m0-
3
Cro
tala
ria
avon
ensi
sFl
orid
a sc
rub
5-30
b%
flow
erin
g,
dens
it y1
58
10 x
10m
, 10
x 15
m0-
2
Dic
eran
dra
frut
esce
nsFl
orid
a sc
rub
5-30
bde
nsity
3-
291
x 1m
0-2
Erio
gonu
mlo
ngifo
lium
var.
gnap
halif
oliu
m
sand
hill,
Flo
rida
scru
b1-
5a , 5-3
0bde
nsity
5-
1510
x 1
0 m
1-7
Eryn
gium
cun
eifo
lium
Flor
ida
scru
b5-
30b
# pl
ants
17
12-
1-18
Liat
risp
rovi
ncia
lissa
nd d
une,
coa
stal
un
der2
0ye
ars
dens
ity1
21
310
Liat
ris p
rovi
ncia
lis,
scru
bun
der2
0 ye
ars
dens
ity1
2-
-1-
3,10
Linu
m a
reni
cola
pine
rock
land
2-15
cde
nsity
13
2550
x 2
m0-
8
Mar
shal
lia ra
mos
asa
ndhi
ll1-
5a#
flow
erin
g pl
ants
19
--
0-4
Nol
ina
britt
onia
nasa
ndhi
ll1-
5a%
flow
erin
g2
416
10 x
10,
5 x
5 m
1-6
Nol
ina
britt
onia
nasa
ndhi
ll1-
5ade
nsity
25
1010
x 1
0, 5
x 5
m0-
4Pr
unus
gen
icul
ata
sand
hill
1-5a
# pl
ants
221
--
1-10
Rhyn
chos
pora
flor
iden
sis
pine
rock
land
2-15
cfr
eque
ncy
13
2450
x 2
m0-
8
Ribe
s ech
inel
lum
mix
ed d
ecid
uous
ha
rdw
ood
fore
stun
der 2
0 ye
ars
dens
ity, %
re
prod
uctio
n1
313
30 x
1 m
, 50
x 1
m1-
3
War
ea c
arte
risa
ndhi
ll1-
5a#
plan
ts1
39-
-0-
3a G
litze
nste
in e
t al.
1995
, b Men
ges 2
007,
c Snyd
er e
t al.
1990
. The
bur
n in
terv
al fo
r Flo
rida
scru
b (5
-30
year
s) in
clud
es a
ll sc
rub
type
s des
crib
ed b
y
M
enge
s (20
07).
Tab
le 1
. Sp
ecie
s an
d va
riab
les
used
in
this
stu
dy.
“Mon
itor
ed h
abit
at(s
)” i
s th
e ha
bita
t in
whi
ch t
he s
peci
es w
as m
onit
ored
. Var
iabl
es t
hat
wer
e te
sted
are
lis
ted
wit
h th
e nu
mbe
r of
pre
serv
es o
r po
pula
tion
s (#
Pop
), n
umbe
r of
man
agem
ent
area
s, b
urn
unit
s or
bas
elin
es (
# B
U),
the
num
ber
of s
ampl
ing
unit
s (#
SU
), t
heir
siz
es (
SU s
ize)
, an
d th
e nu
mbe
r of
ye
ars
pre-
and
pos
t-bu
rn t
hat
wer
e an
alyz
ed.
Volume 30 (1), 2010 Natural Areas Journal �
Preserve(Figure1).
FourofthemonitoredspeciesareendemictosouthFloridapinerockland,whichhasalimestonesubstratewithshallow,droughty,and sandy soils (Table1).Thehabitat isfiremaintainedwithanhistoricfrequencyofeithereverytwotothreeyears(basedonthetimeit takesforfuelstoaccumulate)orevery10to15years,anestimateofthetime it takes forherbaceousendemics tobe shaded by a closed canopy (Table 1)(Snyderetal.1990).TerrestrisPreserveisan8hapinerocklandhabitatinafreshwatermarshcommunityoncentralBigPineKey,MonroeCounty,Florida.
Finally, we use data from two rare spe-cies occurring in hardwood forests andin coastal habitats (Table 1). The MaysPondconservationeasementsite,JeffersonCounty, isadeciduous,mixedhardwoodforestinproximitytothenortheastshoreofLakeMiccosukeethatburnsinfrequently(G.Seamon,FireTrainingSpecialist,theNature Conservancy, pers. comm. 2007)andcontainstherareRibes echinellum (Co-ville)Rehder.TheNatureConservancy’sJohnH.PhippsPreserveisontheeastern-mostcoastalbarriershorelineinFranklinCounty where Liatris provincialis R.K.Godfrey occurs.This species was moni-toredonsanddunesandadjacentcoastalscrub habitat (Figure 1). The habitat isfurther described as evergreen oak-sandpinescrubbyGodfreyandWard(1979).Thesecoastalscrubhabitatsaresubjectedto frequent storm activity (flooding andwinds)andhavehypothesizedmodalhis-toricalburnfrequenciesofunder20years (Schmalzer2003).
Species and Data Collection Methods
All of the 18 species, except for Rhyn-chospora floridensis (Britton ex Small)H.Pfeiff,arestatelistedasendangeredinFlorida(Table1)andallbutfourspecies(Bigelowia nuttallii L.C.Anderson,Mar-shallia ramosa BeadleandF.E.Boynton, Ribes echinellum (Coville) Rehder, and Rhynchospora floridensis (Britton exSmall) H. Pfeiff are Florida endemics.Speciesweremonitoredfordifferenttraitswithvaryingpopulationandplotsizesand
weresubjectedtooneormoreprescribedburnsatvarioustimesduringmonitoring.MonitoringsitelocationsareinFigure1.
Bigelowia nuttallii L.C. Anderson, Nut-tall’sraylessgoldenrod,isanherbaceousperennial foundon the coastal plain andpiedmont of Georgia and Florida, theCumberland Plateau ofAlabama, and incentralandwesternLouisianaandeasternTexas.Thespeciesisfoundinfourlocalizedpatches in sandhill at TNC’s Rock HillPreserve(RHP).Weusedrestrictedrandomsamplinginsevensub-populationstoplacethree30-mx1-mbelttransectswithineachsub-population. We then counted repro-ductiveandnon-reproductiveplantseachSeptember annually from 1992 to 1995andthereafterbienniallyto2001.
Bonamia grandiflora(A.Gray)Hallierf.,Floridabonamia,isanendemictoFloridaandaperennialherbaceousvine.Wean-nually censused two sub-populations insandhill at TNC’s Tiger Creek Preserve(TCP)andtwosub-populationsatSaddleBlanket Scrub Preserve (SBSP) from1991-1997and taggedeachplant.Everyyear we re-located each individual andtaggednewindividualstoderivesurvivalandrecruitmentrates.
Chamaecrista lineata (Sw.) Greene var. keyensis (Pennell)H.S.IrwinandBarneby,BigPinepartridgepea, isanherbaceousperennialendemictoFlorida’spinerock-land habitat. We used restricted randomsampling to establish multiple 2-m widepermanentbelt transects ineachof threeburnunitsonTNC’sTerrestrisPreserveonBigPineKey.Startingin1993,wecountedindividuals annually along the2-mwidebelt transectsso thataveragedensityperm2couldbedetermined.
Chamaesyce deltoidea (Engelm. ExChapm.)Small subsp.serpyllum (Small)D.G. Burch, wedge spurge, is an her-baceous perennial endemic to Florida.We used restricted random sampling toestablish multiple 2-m wide permanentbelt transects ineachof threeburnunitsonTNC’sTerrestrisPreserveonBigPineKey. Starting in 1993, we recorded fre-quencyofthisspeciesincontinuous2-mx1-mplots.
Conradina brevifolia Shinners, short-leaved rosemary, is a shrub endemic toFlorida scrub. In 1999 at TNC’s SaddleBlanket Scrub Preserve, we estimateddensity annually in three permanent 15-m x 2-m plots randomly located withinthepopulationineachoffourburnunits.An additional five plots on the Preservewere added and sampled annually from2000-2003.
Conradina glabra Shinners,Apalachicolarosemary,amint,isanendangeredshrubendemictonorthFloridasandhill.Wesetup three permanent burn units at TNC’sApalachicolaBluffsandRavinesPreserveintowhichwetranslocatedpropagatedcut-tings in 1991 (Gordon1994).Beginningin 1992, we found and tagged naturallyestablishingseedlingsin45oftheexperi-mentallylocated3-mx3-mplotsineachburn unit annually. We stopped taggingnewrecruitsafter1995,butwecontinuedto census all taggedplants until 2002 todeterminesurvivalrates.
Crotalaria avonensis Delaney andWun-derlin, tortoise bells, is an herbaceousperennial,endemictoFloridascrub.From1992to2005,wesampledallplantswithinrandomlylocatedpermanent10-mx10-mor10-mx15-mplotsineachoffivesub-populationsatSBSP.Wemappedindividualplants annually to track recruitment andfloweringcondition.
Dicerandra frutescens Shinners, scrubbalm,isashrubendemictoFloridascrub.Wemarkedallindividualplantsat11sitesatABSandhavefollowedplantsurvival,growth,andrecruitmentsince1988,whichhasledtoarecentassessmentofpopulationviability(Mengesetal.2006).
Eriogonum longifoliumNutt.var.gnaphali-folium Gandog., scrub buckwheat, is anherbaceousperennialendemic toFloridascrub. From 1989 to the present, wemonitoredsixsub-populationsinfourburnunitsatABS,leadingtoanassessmentofpopulation viability (Satterthwaite et al.2002). Within each sub-population, weestablishedbetweenfourand14permanent10-m x 10-m plots, in which all scrubbuckwheat plants were tagged and cen-susedannually.Oneadditionalpopulation
� Natural Areas Journal Volume 30 (1), 2010
hasbeenmonitoredincircularpermanentquadrats (3m radius) at theLakeWalesNational Wildlife Refuge (Carter Creektract)since2001.
Eryngium cuneifolium Small, wedge-leavedbutton-snakeroot,isanherbaceousperennialendemictoHighlandsCountyinFloridascrub.Wehavecensused11sub-populationsandmarkedallindividualsatABS annually since 1988, leading to anassessmentofpopulationviability(MengesandQuintana-Ascencio2004).
Linum arenicola (Small) H.J.P. Winkler,or sand flax, is an herbaceous perennialendemictosouthernFloridapinerockland.We used restricted random sampling toestablish multiple 2-m wide permanentbelt transects ineachof threeburnunitsonTNC’sTerrestrisPreserveonBigPineKey. Starting in 1993, we counted indi-vidualsalongthe2-mwidebelttransectsannually so that average density per m2
couldbedetermined.
Liatris provincialis R.K. Godfrey, God-frey’sblazingstar,isanherbaceousperen-nial, endemic to the Florida panhandle.From1996-2002,wecensusedtwocoastalsandhillburnunitsatJohnS.PhippsPre-serveinthefallofeachyear(except1998)totrackpopulationsize.
Marshallia ramosa BeadleandF.E.Boyn-ton,pinelandBarbarabuttons,isaperennialherbknownfrom20-30sitesinsouthcen-tralGeorgiaandnorthwesternFlorida.WeannuallycensusedallMarshallia ramosaindividuals and the number of floweringindividualsineightsandhillburnunitsfrom1992-2002atRockHillPreserve.
Nolina brittoniana Nash, Britton’s bear-grass,isanherbaceousperennial,endemictoFloridathatoccursinscrubandsandhills(Mengesetal.2006).From1991to2001,wehaphazardlysetupfivepermanent10-mx10-mmonitoringplots inburnunitsatTigerCreekPreserveandtaggedplantsannually(except2000)totrackrecruitmentandflowering.
Prunus geniculata R.M. Harper, scrubplum, is a shrub endemic to sandhill onFlorida‘s LakeWales Ridge. From 1991
to 1996, we tagged all individual plantsannually to track population size at theTiger Creek and Crooked Lake SandhillPreserves.Wealsorecordedthepresenceofreproductivestructuresforeachplant.
Rhynchospora floridensis (Britton exSmall)H.Pfeiff,Floridawhite-top,isanherbaceous perennial found in about 49pinerocklandsitesinFlorida(NatureServe2006)andotherwiseknownonlyfromtheBahamas (Godfrey and Wooten 1981).We used restricted random sampling toestablish multiple 2-m wide permanentbelt transects ineachof threeburnunitsonTNC’sTerrestrisPreserveonBigPineKey. Starting in 1993, we recorded fre-quencyofthisspeciesincontinuous2-mx1-mplots.
Ribes echinellum (Coville)Rehder,Mic-cosukeegooseberry,isawoodysub-shrubknown from two mixed hardwood sitesin Jefferson County, Florida, and fromone site in McCormick County, SouthCarolina. We annually monitored plantdensity from 1992-2001 in eighteen 50-mx1-mandtwo30-mx1-mpermanentbelttransectslocatedthrougharestrictedrandomizationprocessattheMay’sPondsiteinnorthFlorida.
Warea carteriSmall,Carter’smustard,asandhillandFloridascrubendemicfoundon the Lake Wales Ridge, is an annual.Previous work on this species demon-stratedthatpopulationsarereleasedfromtheseedbankfollowingfire,anddeclineprecipitously thereafter (Menges andGordon 1996). We annually censusedthis species during peak flowering inTiger Creek Preserve sandhill. Startingin 1991, we recorded the total numberof plants per sub-population. Sites werecarefullysearchedeachyearandallnewsub-populationsweremapped.Atotalof66 sub-populationshavebeenmonitoredatTigerCreekPreserve.
Data Analysis
Atotalof24variablesfor18speciesweretested.Twelvevariablesweretestedwithrepeatedmeasuresanalysisofcovariance(RMANCOVA)and12weretestedwithanalysis of variance (ANOVA). Multiple
variablesweretestedforfivespecies(Table1).RMANCOVAwasusedtoexaminetherelationship between time since fire andabundanceorvitalrates(e.g.,survivorshipand reproduction) of 10 of the species(Figures2and3).Whereavailable,aco-variatewasusedtoexaminethevariationexplained by pre-burn (sometimes long-unburned,definedas>10yearssincefire)conditions.Covariatedatawasexpressedas density, plant numbers, frequency, orpercentflowering(dependingonthetrait(s)measured for each species).All assump-tionsassociatedwithRMANCOVAweretestedandweremet.Dataweretransformedas necessary to meet the assumption ofnormality.GraphsforvariablestestedwithRMANCOVAshowtheresponsevariableon the y-axis, with the covariate at zeroyearsinceburn(Figures2and3).
Wherewehadinsufficientpost-orpre-burndata to run RMANCOVA (12 variablesof eight species), we usedANOVA. Wetransformed the12 responsevariables toa percentage by calculating the percentchangefromoneyeartothenext,startingfrom zero year since burn. The percentchange for thevariable is againgraphedstartingwithoneyearsinceburnontheyaxis(Figures4and5).Usingthepercentchangeoftheresponsevariablefromoneyear to the next reduces the potentialeffects of pseudoreplication (Wiens andParker1995).
SignificancewasdeterminedattheP<0.05levelforallstatisticaltests.Themonitoringsite,population,orquadrat(ifapplicable)wereincludedasfixedeffectsforalltests.A positive response was identified byeither a significant initial increase in theresponsevariableafterfirethatmayormaynotbefollowedbyadeclineoraninitialdeclineafterfirefollowedbyalonger-termincrease. A neutral response to fire wasdetermined if response was independentoftimesincefire(P>0.05),andanega-tiveresponseoccurredwherepopulationsdeclinedsignificantlyafterprescribedfireandshowednorecovery.
Wehadnopre-firedataforthreespecies:Bonamia grandiflora,Eryngium cuneifo-lium, and Prunus geniculata (Table 1).Monitoring for these species started one
Volume 30 (1), 2010 Natural Areas Journal �
Figure 2. Species whose variables (A through F) were analyzed with repeated measures analysis of covariance (P < 0.05). The value separated from the line at 0 year since burn represents the covariate value: the pre-burn or long-unburned population condition. All graphs shown are ± 1 SE. Number above or below error bar denotes sample size. Where mean change obscures significant trends, population responses are shown separately. Significant p-values are italicized. Variable A = Bigelowia nuttallii density, B = B. nuttallii percent flowering, C = Chamaecrista lineata var. keyensis density, D = Chamaesyce deltoidea subsp. serpyllum frequency, E = Conradina brevifolia density, F = C. glabra density.
10 Natural Areas Journal Volume 30 (1), 2010
Figure 3. Species whose variables (A through F) were analyzed with repeated measures analysis of covariance (P < 0.05). The value separated from the line at 0 year since burn represents the covariate value: the pre-burn or long-unburned population condition. All graphs shown are ± 1 SE. Number above or below error bar denotes sample size. Significant p-values are italicized. Variable A = Crotalaria avonensis percent flowering, B = C. avonensis density, C = Dicerandra frutescens density, D = Marshallia ramosa number of flowering plants, E = Nolina brittoniana density, and F = Warea carteri number of plants.
Volume 30 (1), 2010 Natural Areas Journal 11
yearafterprescribedburn.Therefore,forthesethreespecies,apositiveresponsewasstatisticallysignificantatP<0.05wherethe population(s) showed an increasingtrendsincetheburn.
RESULTS
RM ANCOVA Results
Chamaecrista lineatavar.keyensisdensitysignificantlyincreasedafterfire,withsig-nificantsiteandcovariateeffects.Thesiteeffect (P = 0.0017) (Figure 2C) resultedfromincreaseddensityof thepopulationinunit2 fromthe third through thefifthyearafterburning,whileunit1showednochangeovertime.
Data were limited to the first two yearsafter burning for two scrub species thatexhibitedsignificantandpositiveresponsestofire.Crotalaria avonensisflowering(P= 0.0023) (Figure 3A) and Dicerandra frutescensdensity(P=0.0067)(Figure3C)increased the second year after burning.Wehadthreeyearsofpost-burndataforConradina glabra,whichshoweddensityincreasesinyearstwoandthreeafterfire(P = 0.0013) (Figure 2F).This responsevariedamongthesites(P=0.05)(Figure2F). Three years of post-burn data forWarea carterinumbers showedadramaticincrease one year post-burn followed bya sharp decline in the second year (P =0.0474) (Figure 3F). Species for whichwehadlongerpost-burnintervalsincludedConradina brevifolia,whichshoweddra-maticincreasesinplantdensitythesecondyearafterburningandcontinuedtoincreasethroughfiveyearsafterfire(P<0.0001)(Figure2E).
Traitsofthreespeciesshowedasignificantdependenceontimesincefire(P<0.05),but had non-significant overall models.These were frequency of Chamaesyce deltoidea subsp. serpyllum (P = 0.1068)(Figure2D),densityofBigelowia nuttallii(P=0.8683)(Figure2A),anddensityofCrotalaria avonensis (P=0.1223)(Figure3B).Neitheryearsinceburnnoranyothermodel variable significantly affected thepercentfloweringofBigelowia nuttallii (P=0.2066)(Figure2B),numberofflowering
plantsofMarshallia ramosa(P=0.2911)(Figure3D),ordensityofNolina brittoni-ana (P=0.3708)(Figure3E).
ANOVA Results
Threeoftheninespeciesshowedsignifi-cantpositivedependenceofpercentchangeinvital ratesor abundance traits onfire.Eryngium cuneifolium density increased(P=<0.0001)(Figure4E)graduallyuptosixyearspost-burnandremainedathighpopulationnumbersforaboutsixtonineyearspost-burn,beforegraduallydeclining.Eriogonum longifoliumvar.gnaphalifolium densityincreasedsignificantly(P<0.0001)(Figure4D)oneyearpost-burn,followedby a sharp decline thereafter. AlthoughsitefactorsweresignificantforbothtraitsmeasuredforRibes echinellum,percentre-productionincreasedthesecondyearafterburning(P=0.0096)(Figure5F);densityincreasedsteadilyforthreeyearsafterburnalthough no significant fire-dependencewasfound(P=0.2182)(Figure5E).
Sixofthespeciesshowednostatisticallysignificantresponsetoyearsincefire.Traitsfollowedforallthesespecieswerestableorshowedsomerecoveryafterprescribedburns.Numberofplants(P=0.4916)(Fig-ure4A),percentreproduction(P=0.1018)(Figure4B),andnumberofrecruits(P=0.0699) (Figure4C)ofBonamia grandi-florawereindependentoffiremanagement.Responses were also not significant fordensityofLiatris provincialis(P=0.6716)(Figure4F),percentfloweringofNolina brittoniana (P=0.3371) (Figure5B),ornumberofplantsofPrunus geniculata(P=0.6091) (Figure5C).Finally, twopinerockland species showed no statisticallysignificanttrends;neither Linum arenicoladensity (P = 0.0968) (Figure 5A) norRhynchospora floridensis frequency (P= 0.3790) (Figure 5D) changed over thedurationmonitored.
DISCUSSION
Across all species and life history traits,variablesfornineofthe18species(50%)showed statistically significant positiveresponses to fire, and variables for ninespecies (50%) showed neutral responses
to fire. Responses varied across species,traits, and sites (Figures 2, 3, 4 and 5).Nospeciesshowedasignificantlynegativeresponsetofire.
Plant Adaptations to Fire
This work contributes to the growingdocumentation of fire requirements forviability of species. Post-burn resprout-ing and obligate seeding in other fire-dependent communities have been welldocumented,includingtheMediterraneanBasin (Canadell et al. 1991; Lloret andLópez-Soria 1993; Pausas 1997; Quin-tana et al. 2004),Australia (Zammit andWestoby 1987; Benwell 1998), southernCalifornia (Keeley and Zedler 1978;Moreno and Oechel 1993), the southernAndes (Burns1993), southeasternBrazil(CirneandScarano2001),incircum-borealforests (Rowe 1983; Goto et al. 1996),andinSouthAfrica(HolmesandNewton2004).However,suchmechanismsoffireadaptationhavereceivedlessattentioninFlorida’spyrogenichabitats.
Recentworkhasdocumentedmechanismsthat contribute to species survival andviability in Florida scrub (Menges andKohfeldt1995;Carrington1999;Weekleyand Menges 2003; Menges 2007), sand-hill(MengesandDeyrup2001;Mulliganand Kirkman 2002), and pine rockland(Liuetal.2005;LiuandMenges2005).Adaptations that allow species to persistinhabitatsthatburnincludetheabilitytosurvive high temperatures and resproutaftertissueloss.Forexample,thepredomi-nantpinesofsandhillsandpinerocklands,Pinus palustris P. Miller (longleaf pine)and Pinus elliottii var. densa Little andDorman(Floridaslashpine),respectively,havemorphologicaladaptationsthatconferresistance to frequent, low intensityfires(MengesandDeyrup2001).Thegrowingmeristems of seedlings of both speciesareprotectedclosetothegroundwithinadense clusterofneedles.As adults, bothalsoshedlowerbranchesanddevelopthicklayersofbark.
Threespecieswedocumentwithsignificantresponsestoburninghavebeendemonstrat-edtoresproutaftertissuelossfromfireorotherdisturbance.Oneplantspeciesnative
12 Natural Areas Journal Volume 30 (1), 2010
Figure 4. Species whose variables (A through F) were analyzed with analysis of variance using percent change data (P < 0.05). All graphs shown are ± 1 SE. Number above or below error bar denotes sample size. Significant p-values are italicized. Variable A = Bonamia grandiflora number of plants, B = B. grandiflora percent reproduction, C = B. grandiflora number of recruits, D = Eriogonum longifolium var. gnaphalifolium density, E = Eryngium cuneifolium number of plants, and F = Liatris provincialis density.
Volume 30 (1), 2010 Natural Areas Journal 13
Figure 5. Species whose variables (A through E) were analyzed with analysis of variance using percent change data (P < 0.05). All graphs shown are ± 1 SE. Number above or below error bar denotes sample size. Significant p-values are italicized. Variable A = Linum arenicola density, B = Nolina brittoniana percent flowering, C = Prunus geniculata number of plants, D = Rhynchospora floridensis frequency, E = Ribes echinellum density, and F = R. echinellum percent reproduction.
1� Natural Areas Journal Volume 30 (1), 2010
tosandhills,Conradina glabra, respondstofrequentfirebyresproutingandrecruit-ingfromseedafterfireandisresilienttoa range of fire return intervals (Gordon1994; Menges 2007). Carrington (1999)reportedthatEriogonum longifoliumvar.gnaphalifolium resprouts and flowers inresponsetofireandhasstrongpost-burnseedlingestablishmentresponseswithin19monthspost-burn.Increasesinreproductiveoutputofthisspeciesresultfromincreasedfloweringfollowingfire(Satterthwaiteetal.2002).McConnellandMenges(2002)noted that seedling establishment of E. longifoliumvar.gnaphalifoliumincreasesinburnedareasduetolitterremovalasaresultofburning.Crotalaria avonensiscanresproutafterlowintensityfire(B.Pace-Aldana,MonitoringBiologist,TheNatureConservancy, pers. comm. 2008). ThisworkdemonstratessignificantincreasesinfloweringofC. avonensisthesecondyearafterburning.Morepost-burndatawouldbeidealfordocumentingfurthertrends.
Speciesseenheretohaveneutralresponsestofirehavebeendocumentedtoresproutinotherstudies.WeekleyandMenges(2003)describedBonamia grandifloraasastrongresprouterwithnosignificantdifferencesinrecruitmentpre-orpost-burn.HartnettandRichardson(1989)reportedincreasedreproductionandplantdensityofBonamia grandiflora in recently burned plots viaseedlingrecruitmentandresprouting.Wefoundno significant recruitmentofBon-amia grandiflora after burning, althoughourlowsamplesizemayhaveinfluencedthe result.Wealso foundnon-significantchange inbothplantdensityandflower-ingofNolina brittonianaandnumberofplants of Prunus geniculata with timesince burn.Weekley and Menges (2003)reported 98% survival of tagged Nolina brittoniana individuals and significantlyhigherpost-burnstemdensitiesofPrunus geniculata.Asseeninthisstudy,firedidnotresultinincreasedmortalityineitherspecies(WeekleyandMenges2003).
Otherspeciesinthesepyrogenichabitatsrespondsimilarlytofire(Table2),whichcan stimulate resprouting and flowering(Abrahamson1984a;Kirkmanetal.1998;Carrington1999;Yahretal.2000;Norman2003), especiallyaftercoolerfires(Spier
andSnyder1998),increasecover(ReinhartandMenges2004),andincreaserootandrhizome to shoot ratios (Hartnett 1987).Post-burnstimulationoffloweringinsomespeciesmaybedelayedforseveralyears(OstertagandMenges1994).
Otherspeciesarepost-burnobligateseed-ersthatarekilledbyfirebutrecruitfromseedbanks(Table2).Demographyofthesespecies can provide information aboutlikelynaturalfirereturnintervals(Menges2007). Longer-lived species that recoverfromseedbanksfollowingfireshouldbebetteradaptedtosystemswithlongerfireintervalsthanshouldrelativelyshort-livedperennials. Johnson (1982) hypothesizedthatfirereturnintervalsshorterthanabout10yearsmayeliminateCeratiola ericoides Michx.(Floridarosemary)fromscrubsites.Additionally, demographic transitions ofsome species are affected by time sincefire (Evans et al. 2008). Multiple matrixpopulationmodels,deterministicanalyses,andstochasticsimulationsofChamaecrista lineata var. keyensis demonstrated thatrecentlyburnedsites(1–2yearspost-burn)had the highest finite population growthrates in this species of all sites (Liu etal.2005).
Fire Management Implications
HabitatneedsofwildlifespeciesinFloridaalsosuggestthehistoricalfrequencyoffireforassociatedplantcommunities.Aphelo-coma coerulescens(Bosc,1795),orFloridaScrub Jay, often abandons habitat afterscrubvegetationexceeds threemeters inheight(WoolfendenandFitzpatrick1984;Schmalzer et al. 1994; Breininger et al.1999;Duncanetal.1999)orifsandpineinvadesthesite(WoolfendenandFitzpat-rick1984).Speciesfoundinsandhillandflatwoods require groundcover and openmidstories maintained within relativelyfrequentfire.ExamplesincludeGopherus polyphemus (Daudin, 1802), or GopherTortoise, which requires sufficient coverofherbaceousforagefoundinopenpine-lands(Breiningeretal.1994;Hermannetal.2002),andPicoides borealis (Vieillot,1809), the Red-cockaded Woodpecker,whichalsorequiresanopenmidstory(Ho-visandLabisky1985;Kellyetal.1994;Jamesetal.1997).Severalspeciesoccurin
habitatswithsignificantcoverofbaresoil,includingFloridaScrubJay(WoolfendenandFitzpatrick,1984),Sceloporus woodiStejneger,1918,orFloridaScrubLizard,andNeoseps reynoldsiStejneger,1910,orSandSkink(Greenbergetal.1994;Branchetal.1999;Gianopulos2001;Greenberg2002).
Evenwherefiremanagementremainsanactive practice, providing a variable ordiversefireregimemayhelpbenefitcon-servationofecosystemsinFlorida(Abra-hamson1984b;RobbinsandMyers1992;SpierandSnyder1998;Liuetal.2005).In the last century, prescribed burners,especiallythoseburningwithsilviculturalorrangelandgoals,concentratedonwinterburnstofacilitatefiremanagementandre-juvenatespringforage(RobbinsandMyers1992; Miller andWade 2003). However,morenaturalgrowingseasonburnsarees-sentialforcertainplantspecies.Severalofthosespeciesshowingneutralresponsestoprescribedfiremanagement in thisstudywereburnedmainlyinthewinterorearlyspring(Bigelowia nuttalliiwasburnedinFebruary,Marshallia ramosa wasburnedinFebruaryandMarch,and Nolina brit-toniana wasburnedfromOctoberthroughMarch).Thetimingofthesefiresmayhavebeeninsufficienttostimulatetheresponsesdescribedabovethatshouldhavefacilitatedpositiveresponsestofire.
Fire Surrogates
Today, prescribed fire for conservationand agricultural purposes now generallyreplacesthenaturalandhistoricsourcesoffire(RobbinsandMyers1992).ArecentanalysisbytheFloridaDivisionofForestryandtheFloridaParkServiceidentifiedasmuchas40%(104,836hectaresof262,090managedhectares)offire-dependanthabi-tatsmanagedbyFloridastateagenciestobefiresuppressed(Hardin2002).Difficultyoffiremanagementinanincreasinglydevel-opedlandscapeisresultinginsubstitutionofmechanical(mowing,chopping,disking)and herbicide approaches for vegetationmanagement.
These fire surrogates have been used topreparesitesforprescribedburnsorreplaceburningentirelywhenitisconsideredno
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longerfeasible.Clear-cuttingandsalvagelogging of Pinus clausa (Chapman exEngelmann)Sargent(sandpine)inscrub(Greenberg et al. 1996; Provencher etal. 2000), hardwood reduction usingherbicides and chain-saws in sandhills(Provencher et al. 2001), stand thinningin pine rocklands in southern Florida
(Maschinskietal.2005),andchoppingormowinginhabitatsfromflatwoodstodryprairietoscrub(Wattsetal.2006;Willigesetal.2006)haveallbeenused tomimicthe structural and fuel reduction impactsoffirewithsomemeasureofsuccessforsomespecies.However,theseapproachesappearnot tosubstituteforfireforsome
speciesconsideredkeystonetothesehabi-tats.Forexample,AristidastrictaMichx.(pineland threeawn or wiregrass) willflowerinresponsetovariousstresseslikedefoliation and soil disturbance (Parrott1967);however,itneedsasummerburntoproduceviableseed(Duever1989;Outcalt1994).Mechanicaltreatmentsthatarenot
Species Response to fire Habitat ReferenceAristida stricta Michx. Viable seed production Sandhill,
flatwoodsDuever 1989; Outcalt 1994; Mulligan and Kirkman 2002
Calamintha ashei (Weath.)Shinners
Increased seedling recruitment
Carrington 1999
Ceratiola ericoides Michx. Obligate post-burn seed bank
Florida scrub Johnson 1982
Chamaecrista lineata var. keyensi s
Obligate post-burn seed bank
Pine rockland Liu and Menges 2005
Conradina brevifolia Obligate post-burn seedbank Florida scrub B. Pace-Aldana pers. comm. 2008
Dicerandra frutescens Obligate post-burn seed bank
Florida scrub Quintana-Ascencio et al. 2003; Menges and Quintana-Ascencio 2004; Menges, unpublished data
Eryngium cuneifolium Obligate post-burn seed bank
Florida scrub Quintana-Ascencio et al. 2003; Menges and Quintana-Ascencio 2004; Menges, unpublished data
Garberia heterophylla (W. Bartram) Merr. and F. Harper
Resprout, stimulated flowering and recruitment
Florida scrub Carrington 1999
Hypericum cumulicola (Small) P. Adams
Obligate post-burn seed bank
Florida scrub Quintana-Ascencio et al. 2003
Lechea deckertii Small Increased seedling recruitment
Florida scrub Johnson and Abrahamson 1990
Lechea cernua Small Increased seedling recruitment
Florida scrub Johnson and Abrahamson 1990
Palafoxia feayi A. Gray Resprout, stimulated flowering
Florida scrub Ostertag and Menges 2004
Paronychia chartacea Fern Increased seedling recruitment
Florida scrub Johnson and Abrahamson 1990
Pinus clausa (Chapman ex Engelm.) Vasey ex Sarg.
Obligate post-burn seed bank, serotinous cones
Florida scrub Outcalt and Greenberg 1998
Polygala lewtonii Small Increased seedling recruitment
Sandhill U.S. Fish and Wildlife Service 1999; Weekley and Menges unpublished data
Warea carteri Obligate post-burn seed bank
Scrub, sandhill Menges and Gordon 1996
Table 2. Examples of plant species responses to fire in Florida’s pyrogenic habitats from the literature.
1� Natural Areas Journal Volume 30 (1), 2010
followedbyfirefailtoallowrecruitmentof endemic Florida scrub herbs (Rickeyet al. 2007), which is probably due topersistent litter that would otherwise beconsumedbyfire.Withoutunderstandingof the mechanisms behind responses ofspecies like the ones examined here, wecannotbeconfidentthatthesealternativeapproacheswillhavethedesiredeffectsonallcomponentsofthecommunity.
Implications for Future Research and Monitoring
Thedurationofthesemonitoringprojects,eventhosecontinuedforover10years,maybeinsufficienttofullyclarifypatternsofresponsetofire.Thelagtimeobservedforpositiveresponses,especiallyinthescrubspecieswhoseindividualsinitiallydieafterburning,representsthetimeneededforseedgerminationandseedlinggrowth.Longermonitoringandautoecologicalstudiesmayclarifypatternsforthosespeciesthathadinsignificantlypositiveresponsestofireinthis study.Alternatively, chronosequencestudies that monitor populations at mul-tiplesiteswitharangeoftimespost-burnmay be used to infer post-burn patterns(Menges2007).
While these results cannot be used toidentify life-history traits that are morecloselyassociatedwithsignificantpositiveresponse tofire (reproductive traitsweremeasuredforsixofthe18species),severallinesofevidencesuggestthattheabsenceoffireposesamorecriticalthreattoper-sistence of these rare species than doesits presence. Fire exclusion is predictedtocauselocalextinctionofFloridascrubplants (Menges and Quintana-Ascencio2004;Mengesetal.2006).Withincreasedtimesincefire,rareandcommonspeciesas-sociatedwithlongleafpine-wiregrasshabi-tatsmaydecline(Provencheretal.2001;Gray et al. 2003).Without fire, changesin community structure of sandhills willoccur(Mengesetal.1993);suchchangescan be reversed if fire is re-introduced,potentiallyfollowingfuelreductiontreat-ments (Provencher et al. 2001; Reinhartand Menges 2004). While, more studiesmeasuring multiple population variablesinadditiontoabundancemayhelpdefine
associationsofcertainvariablestofireandpossiblyprovidefuturedatasetsforamorecomplex meta-analysis, lack of data onspecificresponsesofindividualrarespeciesto fire in pyrogenic natural communitiesshouldnotprecludefiremanagement.
ACKNOWLEDGMENTS
Thisworkwouldnothavebeenpossiblewithoutthesupportofallofthefieldbi-ologiststhatmonitoredthespeciesonourpreserves.Weareverygratefulforthefieldsupport provided by staff ofThe NatureConservancy and Archbold BiologicalStation.WeespeciallythankC.Bergh,A.Higgins, B. Krieter, B. Pace-Aldana, D.Printiss,P.Quintana-Ascencio,G.Seamon,C. Weekley, and many others who havehelped to collect these long-term data.Wealsoappreciatecommentsfromthreereviewers that improved thismanuscript.SupportfromtheNationalScienceFoun-dation(DEB98-15370,DEB-0233899andDEB-0812717), the Florida Division ofPlant Industry, and the Florida ChapterofTheNatureConservancyaregratefullyacknowledged.
Jodi L. Slapcinsky is a Monitoring Ecolo-gist for the Florida Chapter of The Nature Conservancy. Her current research inter-ests include plant demography and the effects of fire on vegetation, and species and community monitoring and manage-ment in Florida natural areas.
Doria R. Gordon is Associate Director of Science for the Florida Chapter of The Na-ture Conservancy and Courtesy Professor of Biology at the University of Florida. Her research focus includes restoration of fire and species in longleaf pine ecosystems, identification and prediction of invasive non-native plant species, and ecology, conservation, and management of rare species and communities.
Eric Menges is a Senior Research Biologist at Archbold Biological Station. His main research and conservation interests include the biology of rare plants, population vi-ability, fire ecology and management, and restoration ecology. He has published over 110 papers on these topics.
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