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Year: 2017

Conservation value of disturbed and secondary forests for ferns and along an elevational gradient in

Carvajal-Hernández, César I ; Krömer, Thorsten ; López-Acosta, Juan Carlos ; Gómez-Díaz, Jorge A ; Kessler, Michael

Abstract: Questions: How do species richness and composition of fern assemblages change with elevation and, within elevational belts, in differently impacted forest habitats? Is there a relationship between fern assemblages and microclimate, both along gradients of elevation and disturbance? Which species are most sensitive to habitat disturbance and microclimatic changes? Location: The transect starts at sea level close to the Gulf of Mexico and ends 81 km away in a direct line on the eastern slopes of the Cofre de Perote at 3500 m, in central Veracruz, Mexico. Methods: We studied the richness and composition of fern assemblages in 120 study plots at eight elevations at 20-3500 m in three forest types: natural forest (NF), disturbed forest (DF) subjected to timber extraction and grazing, and secondary forest (SF) regrown after total clearance 15-20 years ago. In addition, we measured microclimatic conditions in the three forest types at five elevations over a year. Results: Fern richness peaked in humid montane forests at mid-elevations and was low in the dryer habitats at the ends of the gradient. Humid montane forests were most sensitive to disturbance, showing increases in mean annual temperatures by about 1°C and reduction in relative air humidity by about 20% in DF and SF compared to NF. This went along with a reduction of fern species richness by 5-60% and marked changes in species composition. In contrast, drought-deciduous forests at low elevations and coniferous forests at high elevations already had low humidity and high light intensity in NF and were less affected by human impact: Their microclimatic conditions and fern assemblages did not change markedly in DF and SF. Conclusions: The conservation of much of the humidity-dependent biota (ferns and presumably also groups such as bryophytes and amphibians) in humid montane forests depends on the protection of natural fragments without human disturbance. In contrast, the naturally open forests at the ends of the gradient can be subjected to some exploitation while conserving much of their fern flora as long as a general forest structure is maintained.

DOI: https://doi.org/10.1111/avsc.12318

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-137774 Journal Article Accepted Version

Originally published at: Carvajal-Hernández, César I; Krömer, Thorsten; López-Acosta, Juan Carlos; Gómez-Díaz, Jorge A; Kessler, Michael (2017). Conservation value of disturbed and secondary forests for ferns and lycophytes along an elevational gradient in Mexico. Applied Vegetation Science, 20(4):662-672. DOI: https://doi.org/10.1111/avsc.12318 Kessler, M. Kessler, ([email protected]) Gómez-Díaz, J.A ([email protected]) J.A Gómez-Díaz, López-Acosta, J.C. ([email protected])López-Acosta, J.C. MR. JORGE ANTONIO GÓMEZ DÍAZ (Orcid ID :0000- DÍAZ(Orcid GÓMEZ ANTONIO MR. JORGE Krömer, T.([email protected]) This article isThis article by protected copyright. All rights reserved. 10.1111/avsc.12318 differences thisbetween and Version version the ofRecord. cite Please this asdoi: article the through copyediting,and proofreading process, typesetting, pagination to whichmay lead This article acceptedhas been forpublication andundergone full peer review buthasnot been 0000- ID : (Orcid CARVAJAL-HERNÁNDEZ DR. CÉSAR César I. Carvajal-Hernández, Thorsten Krömer, Juan Carlos López-Acosta, Carvajal-Hernández,Juan Carlos Thorsten Krömer,I. César in Mexico elevational gradient and andConservationvalue of ferns disturbed an for along lycophytes secondaryforests Wulf Monika Dr. Editor: Coordinating Co article :Research type Article Carvajal-Hernández, C. (corresponding autor, [email protected]) C. Carvajal-Hernández, autor, (corresponding Michael Kessler& Díaz

Accepted Article Wulf Monika : Editor -ordinating 2

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2

4

0001 0002 - - 8182 5070 -7584) -4140) 1

Jorge A. Jorge Gómez- ,2

disturbance, disturbance, annual showing increases temperatures in mean 1°Cby about in andreduction the habitatsends dryer most Humid of at gradient. were the montane forests sensitive to Results: atfive overtypes elevations ayear. years ago. 15-20 in thethreeclearance forest Inaddition,measured we microclimatic conditions total totimber grazing, after subjected and extraction andsecondaryforest (SF)regrown elevationseight Methods: of line theVeracruz, on slopes Cofre direct 3500 Mexico. eastern dePerote m,at in central the Location: most are Which species to sensitive disturbancehabitat and microclimatic changes? elevation ferngradients of disturbance?between assemblages and microclimate, and bothalong and, within in differentlyelevational belts, impacted foresthabitats? there arelationship Is Questions: Abstract 10.3 This article isThis article by protected copyright. All rights reserved. journal pageestimate Printed 8008 Zurich, Switzerland 4 3,37073, GöttingenGermany. Goldschmidtstr. Universität Göttingen, 3 C.P. 91000,Xalapa,46, ZonaCentro Veracruz, Mexico. 2 Veracruz, Ayalas/nCol.Castelazo Xalapa, Ánimas, 91190, Industrial Mexico. C.P. 1 Herbario CIB, Instituto de Investigaciones Biológicas, Universidad Veracruzana, Av. Biológicas,Herbario CIB,Instituto Veracruzana,de Investigaciones Dr. Luis Universidad Accepted Article ofandBotany,Institute Systematic Evolutionary University of Zollikerstrasse Zurich, 107, ofGeoscience Faculty Geography, andDepartment Physic Geography,GeorgAugust- of María Morelos José Investigaciones UniversidadCentro de No.44y Tropicales, Veracruzana, Fern richness peaked inhumid at andwaslowinthe montane forests mid-elevations

We studied theWe richness studied and composition of fern assemblages 120study at in plots Th How richness offern dospecies andcomposition assemblages with elevation change e transect starts at sea level close to the Gulf of Mexico and ends 81km away ina e transect at close level starts to andends Gulfsea the ofMexico at 20-3500 m 20-3500 forest types: inthree forest (NF),disturbed natural forest (DF) : 5435 2pages, (6.8pages), table words total 1.5pages, figures tropical mountains. Ferns mountains.(henceforth forsimplicitytropical andlycophytes called ferns and known for yet ecosystems some ferns (Gibson al.2011), little is as and et such taxa globe biodiversity across theHuman is profoundly altering ecosystems impact the associated andtheir Introduction This article isThis article by protected copyright. All rights reserved. SF DF NF : Abbreviations Nomenclature : microclimatic secondary forest changes, words:Key forest as longageneral fern flora structure is maintained. of the besubjectedends at thegradient tosomeexploitation can conserving much while oftheir of the In contrast, fragmentsprotection naturally natural open forests withouthuman disturbance. montane forests on groups bryophytes andamphibians) depends also such as the in humid Conclusions: microclimatic Their conditions andfern assemblages not did markedlychange DFandSF. in had byhumanalready low humidity andhighlightintensity impact inNFandwereless affected andconiferous highelevations atlowelevations forestsat forests contrast, drought-deciduous offern species reduction by and richness marked speciescomposition.5-60% in In changes airhumidityrelative byabout20%in DFcompared alongwitha andSF NF.This to went Accepted with cosmopolitan distribution of their particularly are Ferns suitable forstudies onplant and diversity assemblage composition because scales (Whitmoreregional 1985; etal. & Gentry Dodson 1987;Kessler 2001a; Kreft al.2010). et globe, wheretheycan comprise of upto19%ofthediversity atlocal vascular and highrichnessandplant lineages with montane abundance inhumid forests across tropical the Article = Secondary forest Secondary = = Disturb forest = Natural humid montane humid degraded forest, forest,indicator mature species, forest, ed The conservation of much of the humidity-dependent biota (fernsandpresumablymuch ofThe conservationof humidity-dependent the forest Tropicos: www.tropicos.org

a high but manageable number of 10000-13000 species high butmanageable species number of10000-13000

) are are twomajor : air humidity (Scatena et al. 2005; Sporn humidity al.2009air (Scatena et 2005; et al. as asreduced well goesalonglarge trees, shading that increasing temperatures with and reduced alsodiffer forests,they inimportant ecological traitsnatural fromsuch asa lowerabundance of 2011).Clough conservation Wright ofbiota the & (Dent al. However, forest-dependent et 2009; theiragroforests. Because of dominance suchecosystems oftrees, in may important roles play of but and pastures, to conversion forests alsofields or creation of inthe secondary forests not in Thishas only the al.2011). resulted (Castillo-Campos vegetation outright cover et natural al et (Tejero-Díez ofexample, where state the Veracruz, is home was564 fernspecies ourstudy to conducted, (Kessler 2001b). These previous studies 2001b). ignored two (Kessler largely have These themes: interesting have disturbedslightly montane endemic forests more regionally forests natural ferns than 2014). hasCarvajal-Hernández al. 2009; In contrast, et astudy in Bolivia documented that Prado2005;Rodríguez-Romero & Mehltreter al.(Paciencia 2008; et et 2008;Haro-Carrión al. in richnessloggedin species forests of40-70% andsecondary compared natural forests to losses known ecosystems, non-natural Little is aboutfernsin documented have some but studies al (Kessler et impactand on the ofhuman forestin different types toelevation in activities relation the N the (Salazarlesswhere fernsareverydiverse transition al.2015), diverse et andthe zones between This article isThis article by protected copyright. All rights reserved. 2001a;(Kessler Klugeet 2006;Watkins alal. et strongly richnesstowardslower anddecreasing elevations m, higher ofwith about1500-2000 2008).disturbance and those that aremore (Mehltreter resilient 2002); andbecause contain bothtaxathat factors sensitiveabiotic they are (Page habitat to dispersal spore which limits interactions resultingin biotic more direct relationships towards Smith their of& relative recognition the 2004); in theease (Mickel 2008); globally (Moran field forests found in many regions of and the Andes, are defined are ecosystems as foundinmanyforests ofCentral with America regions Andes, andthe 2005, 2011;Einzmann(Werner al.2016).Natural dry etal. et forests such as drought-deciduous (mainly availability in relative the depending humidity types forests air andrainfall) onthe water itparticular, suggested has been impactthat maythe ofhuman disturbance differ between forest humidity-dependent affectIn especially organisms asferns, such isknown but little this. about .

Accepted 2001) Article eo In tropical mountains, ferns generally show the highest atintermediatethe highest richness In tropical ferns generallyshow mountains, elevations tropic andNeartic, asitoccursincentral an d ii) changes in the diversity changes offerns betweend ii) Neotropic,transition inthe zone in the the . 2014; but Krömer 85%in the lost 2015) of last hasalso etal. its 30 years, . et Kessler al 2006a; Me ). xico (Sánchez-Colón et al. 2009) (Sánchez-Colón etal. xico Such microhabitat changesare likelyto . 2011; et Salazar al . i) For changes changes . 2015). affinities, with tropical oak forest below 1000 m, humid montane withtropicalaffinities, m, oak belowhumid forests 1500-2300 at1000 forest m, vegetation 2011). Thenatural Giddings combines and Nearctic Neotropical elements of linearly with linearly precipitationhighest elevation, is (18° C/1800 mm) at C/800 (9° high C/1800 elevations (18° anddry-cold precipitation:total annual temperature at tohumid-temperate 25°C/800mm and mid-elevations ) This article isThis article by protected copyright. All rights reserved. Acceptedm3500 ( ends 96°22’W) and 1).(Fig. Díaz) The transectManuel starts de median(in and the in the Sierra (within the Actopan andlower parts Sierra Madre Oriental) La Antiguain itshigher part gradient forms of the rivers Theelevational ofthedrainages part Study area and methods Materials and microclimatic changes? of Which anddisturbance? elevation gradients species aremost sensitive tohabitatdisturbance habitatsforest belt, fern assemblages in differently change impactedwith elevation and,within elevational each this of of were:Howdospecies Themain andcomposition richness ecosystems. study questions Article forests. Thiscomparing influenceofsecondary the human different thusallows in impact amix forest contains above3000m. also It elevations disturbed and ofnatural remnants,forests, humidforests low elevations, montane at intermediate elevations andconiferous forestsat This at wide forests gradient Mexico. coversa range ofVeracruz, from habitats, semi-deciduous and ofdiversity patterns assemblage anelevational composition along gradient in central Ramos 2014). Dirzo & microclimaticsusceptible that lead tomajorto (Sánchez- changes alterations of forest structure especiallyforests, montane thosetowards aridity the limit ofthishabitat, appear to be highly speciesaffect the (Carvajal-Hernández greatly richness humid Incontrast, &Krömer 2015). may already adapted stress,by species not towater so ofthat alterations theforest structure are Therefore (Banda inhabited they anda dominancedeciduous of al. species 2016). droughts et prolongedcanopy,a closed with precipitation and than1800 onfertile soils mm less year, per In the present we In the out study, set to quantifythe impact ofhuman disturbance onthe 19°30’

? Is Is athere relationship both fern along between assemblages microclimate, and N , 97°08’ 81 km away in a direct line on the eastern slopes ofon the line Cofre slopes 81kmaway eastern direct the dePerote in a a W). Climate changes from dry-hot at low elevations (average lowelevations W).at changesfrom annual Climate dry-hot at to sea level close Gulf the of Mexico(19 35’N, in the middle of the gradient (Soto-Esparza & the& middle gradient the of (Soto-Esparza mm) . While. temperature decreases t ii) natural by in differentseparated habitats:( forest about 500m three i) 1), (Fig. 2013, 2012toOctober 120 study ateight weestablished elevationalFrom plots belts, February work Field (2500 m); m);ElConejo6. ElEncinal 7.LosPescados(3000 (3500m). Palmarejom); (500 m); 3.Chavarrillo(1000 4.LosCapulines (1600m); m); 5.ElZapotal(2000 Fig. 1 ago, accordingyears tothesome people. comments oflocal 15-20 disturbed forest vegetation aswell andnatural forests secondary as resultingfrom clearcutting At most al.2011). possiblefind both(Castillo-Campos et elevations,to itis remnants ofthe This article isThis article by protected copyright. All rights reserved. Accepted Article transitional disturbed( forest Location of the eight study sites in Veracruz State, sites1. La Veracruz Locationoftheeightstudy State, Mexico. (20 in Mancha m); 2.

Pinus-Quercus DF ) subjected and) toselectivelogging iii) grazingbygoatsorcattle, and forests at 2300-2700 m, and coniferous forests above 2800 m at forests m,andconiferous forests2800 2300-2700 above NF ) notdisturbed, )

comparison was made considering the species turnover from from turnover SF,aswell DFNFmadecomparison toDFand thespecies was considering (ANCOVA habitatsdifferent each belts in oftheelevational differentbetween andbetween elevations assessthe threeturnover ofspecies 2010) to the hemispheric photographs. data loggers by andcanopythe obtained andlight openness transfer that were obtained from the Moreover,was calculated aSpearman between valuesand light intensity. the correlation daily mean thenSimilar for analyseswere conducted oftemperature, relative values humidity, with elevationalthe Tukeya transect hoc post to three respect test. habitat the and with types, ANOVAWe anested if used were totest there per alongdifferences inthespeciesrichness plot Data analyses tomeasurewere taken the openn canopy m light intensity logger These 2-3 complete data placed dueto failure). were data a trunksat ontree humidity and record onethat entire gradient; in all three habitats loggerstwo thatrecordin gradient;we all placed data three habitats entire m,types present3500 m), fiveand whichrepresent ofvegetation m, different the the 2500 along m, m, (January 30 (500 one year toDecember five every elevations at minutes 1500 1000 2014) for humidity, relative as welllight (HOBO PendantTemperature/Light DataLogger) intensity of or and/ University California theInstitute Xalapa. (UC), Berkeley of Ecology,A.C.(XAL), ofVeracruz City,Xalapa, (CIB), University as theMexico aswell partially in herbaria of the Nationalwere deposited the in Herbarium ofBiology oftheInstitute (MEXU) of UNAM, the up The(presence/absence) ofaboutto m a height specimens eight (Krömer 2007). collected etal. (NF, habitat plot, all werecorded Ineach terrestrial ones DF, SF). ferns andepiphytic Bach & m with plotsof 1999), establishing fiveplots 20 x (Kessler 15 study in each each acahuales acahuales This article isThis article by protected copyright. All rights reserved. forests( secondary

Accepted hemispherical all plots Inaddition, lens in photographsabove the ground. through a"fish eye" Article We used Whitaker’s indexWe used We placed 42 microclimate data loggers (HOBO We 42microclimate PRO temperature and placed air torecord dataloggers v2) elevational At each belt, in systematica sampling whichconsisted performed, was (Romero al. et 2000 ) to assess elevational and habitat-dependent differences inbeta and diversity habitat-dependent to assess elevational

SF ) regenerating after clearcutting some 15-20 years some years ago, regenerating clearcutting knownafter locally 15-20 as ed ). light intensity light 3500mintensity (however,get in the wasnotpossible it to

of beta diversity (Whitaker of 1960; diversity beta Tuomisto Koleff al.2003; et ess and transfer of light into andtransferoflightinto the understory. . We then used a generalized linear modelWe ageneralized linear used then ed temperature and (t his presentation, the values at a given elevation are slightly shifted inelevation. slightlyshifted presentation, values the atagiven elevation are sites along SF: secondaryforest) attheelevational the forest; eightstudy gradient. For clarity of 2 Fig. at forest 500m. deciduous This article isThis article by protected copyright. All rights reserved. and classification (information ontaxonomic 120study 62genera and24familiesIn the we to belonging plots, 155 recorded of species ferns richnessSpecies Results R 3.1.2). (Development Coreteam; version analyses (Dufrêne atIndVal Legendre& 1997) elevation thepackagelabdsveach in using 1.5-0 ToCórdoba, Argentina). identify species indicator for habitats, different the weconducted using 2015 program Nacionalde to SF), the InfoStat,FCA,Universidad Infostat (Grupo humid montane followedhumid forest, bythe transitional was 3500 thus withmaximum 2). m) species at (Fig. The forest richness the type m andsix (62 species) Accepted ArticleKrömer 2015 Patterns of in species richness the forest three types (NF: natural forest; DF:disturbed

, whereas plots at the ends much plots had of gradient at the whereas the (fourspecies 20 at fewer species ). Species Species richness peaked 1500 at m (67species in total in 15plots) all and 2000m

a species list arespecies list available Pinus-Quercus Pinus-Quercus forest semi- m)forest the (2500 and in Carvajal-Hernández & Carvajal-Hernández &

of species richnessof inthe species middle ofthegradient zones and even less no comparisonindicates there DFthat were andSF, significant differences between inthevalues Tukey to the According the test, per wasroughlysimilar threeforest types. in all plot richness the ends as at species manyof gradient plot whereas the SF onlyhad30-53% per as NF, species habitat (nested ANOVA, (nested habitat ANOVA, fewersignificantly than species (nested forestnatural (SF)had (NF) and secondary forests even higher (0.56±0.22) betweenTurnover inNF DFwas plots in andthose higher (0.50±0.23) and NF between andSF turnover between inNFSpecies plots wasfairly beta of,low (Whittaker’s turnoverSpecies gradient. ( model linear The generalised showed species was that turnover influenced both byelevation This article isThis article by protected copyright. All rights reserved. plot than the ends of the gradient (nested ANOVA, of than gradientends (nested the plot the turnover in of habitatsdifferent turnover elevation(ANCOVA, afunction as F

Accepted=7.151 Article In general, theof gradient had middle the part In general, ; F df =44.189; =44.189; = 4 = ; P <0.001) andhabitat type ( df =2; =2; . In general there was a negative linear relationship between the species therewasanegativespecies linearIn general relationship the between F = 2084. 20; = 2084.20; P < 0.001 ). There was There asignificant interaction elevation between and df =1; F P =8.825; =0.001) mid-elevations reflecting that at DF and

F =88.346; =88.346; a df significantly species per higher richness = 2;= P < 0.001). < 0.001). df =21; R at =0.50 P the ends of the elevational theelevational ofthe ends <0.001). (DF) Disturbed on average, 0.38±0.2).on average, ; P <0.001) 3). <0.001) (Fig. Temperature (nested ANOVA,Temperature (nested Microclimate disturbed forest forest disturbed at each elevational belt: belt: each temperature: at elevational in types microclimaticthose differences forestwere significant Also, there between the variables P This article isThis article by protected copyright. All rights reserved. (r=-0.45 agiven forest elevation natural at 3 Fig. intensity: intensity: three foresttypesalongthe gradient. a) elevational three df 0.2°C. The temperature fluctuation between the highest value and the minimum varied according 0.2°C. highest fluctuation between the The temperature varied value minimumand the at elevationshigher NF,mthan (500 except the m)lower and1000 differences where were about <0.001); d) and DF-SF between disturbed forest and secondary forest plots d) forest betweendisturbed DF-SF forest and <0.001); and secondary (r=-0.51; Accepted : 12; Article

Linear regression models of species Linear regression models ofspecies turnover according index toWhittaker’s (β P <0.001), andlight ( intensity F =814.4; =814.4; (r= -0.54; df : 2; P P <0.001. meanOn average, SF had daily temperatures about 0.6°C <0.001); c) <0.001); F =2181.0; =2181.0; F F =209.9; =209.9; =32.7; =32.7; NF ; -SF between NF and secondary (r=-0.43 NFandsecondary forest between -SF df P : 12; <0.001); b) <0.001); b) df df : 2; : 11; P <0.001), relative airhumidity <0.001), ( (RH) NF P <0.001; <0.001; RH: P -NF represents the the comparison-NF represents plotsin of <0.001) changed with elevation (Fig. 4). <0.001) changed with elevation 4). (Fig. NF -DF inNF plots and between F =74.1; =74.1; df : 2; P <0.001; light W P ) for the ) forthe F <0.001). <0.001). ; =236.9; =236.9;

This article isThis article by protected copyright. All rights reserved. however, elevation, to (Table 1 (Table followed by hemispheric photographs show that thehemispheric mo showthat photographs except at 1000 m, where it was similar in all forest types at1000m,(Fig. 4 except wassimilar all forest whereit in types elevations these intensity differences order Light wereonly inthe washighestinSF, of2-4%. 90% SFat about atinNF 69%in intermediate to thehighestandwhereas lowest elevations, Accepted Articleopennessis compared is if correlation positive canopy the between relative correlation openness the humidity canopy and in contrast, the andtemperature; Alongelevational intensity. the gradient observed anegative temperature we and light also found the therewe increased relativepresents decreased largest canopy opening, humidity, middle An example inwhere occurs elevations, ofthis SF NF(13.49%). and DF (17.69%) ).

NF (6.9° C) and finally C)andfinally the (6.9° it showed that showed that on average, DF st showed less fluctuationless RH showed (6.2º C). from declined open canopy occurred occurred in opencanopy SF present to ed theintensitylight and transfer the largest the C), fluctuation (7.05º ). Thevaluesobtained by SF (24.8 %), followed (24.8%), by This article isThis article by protected copyright. All rights reserved. Accepted forest. forest; SF:secondary disturbed Relative ayear:a)Temperature;over b) airhumidity; Lightc) intensity. NF: DF: natural forest; 4 Fig. Article Microclimatic conditions atfive the along elevations study gradient, ondailymeansbased

the disturbed habitats typical disturbedhabitatsthe typical taxa included whereas grammitid such and groups (Pteridaceae), asthe andvittarioidin (Polypodiaceae) ferns (Thelypteridaceae). In the a habitats species-poor (Thelypteridaceae). more information more information ofthe gradientelevational precipitation data regarding Carvajal-Hernández see precipitation (For 2000) isintermediate between recordedat500mvalues and1500m(IMTA indicateattributed tolowstations that be cannot precipitation, nearby datafrom since climatic et(Kessler al.2014).unclear al. Shi-Baomechanistic 2011; link et the 2014), physiology and between species richness isstill Watkins explainthephysiological that 2006b;Brodribb et al. (e.g., aspects of ferns etal (Kreft temperatures theand moderate reflecting physiological requirements offerns forhighhumidity Carvajal-Hernández & Carvajal-Hernández & etKrömer Salazar 2015; al N transition ofthe Kluge al.2001a; reflects et 2006). This thefairly reduction abrupt offern species richness atthe surveys where upto (Kessler beenthree times have many as recorded incomparable species in a context, notable Mexican low this tropicalother richness is relatively areas, compared to This article isThis article by protected copyright. All rights reserved. Amongwith SF. indicator the NF species for (18.7%) NF,2).were with DF,andsix Of23 (71.8%) (9.3%) three associated (Table these, with The IndVal analysis recovered significantly 32species withassociated specificforest types Indicator species known from Mexico (Mickel & Smith 2004; Tejero-Díez etal Smith& Mexico(Mickel 2004;Tejero-Díez known from species currentlyof564 of knownfrom 15% of the the1030species state and the Veracruz The 155fern 4.8 hectare inatotal species recorded 27.5 samplingcorrespond to ofonly area alongtheelevational richness gradient Species Discussion werespecies recovered. Accepted al.Kluge et 2006; Watkins al.2006a et withprevious isconsistent elevationalmid-elevations, (Krömer studies 2005; in the etal. tropics Article A noteworthy from richness departure pattern isthelow overall at1000 m. the This Overall, Overall, the found species richnesspattern elevational maximum byus,with at richness . but 2011; 2010; Kessleret al. etalthough there aresomestudies Salazar 2015), al. eo tropic to the Neartic (Kessler 2000; Moran 2008; Kessler etNeartic al.2011;tropic 2000; (Kessler 2008;Kessler Moran tothe ; Kessler et al. 2011).Kessler etal. isusually interpretedThis pattern as Pteridium we

re members re family Hymenophyllaceaethe of t . 20 m, 1000 m, and 3500 m,20 m,m, 3500 and noindicator 1000 2015 (Dennstaedtiaceae ).

. 2014;Krömer etal ) and Thelypteris Thelypteris . 2015). While 2015). & Mc Adam % This article isThis article by protected copyright. All rights reserved. dominated by species three of natural However, the Krömer vegetation& tree isalso 2015). species fairly poor,being in Veracruz in 2013).and specifically (Torres-Cantú Inother inMexico, regions and 40Fabaceae Asteraceae, in general is high 48species(635 oforchids,with vascularspecies), recorded flora forthe 44 m al.2006; 1500 (Klugeet 2006a). WatkinsInterestingly, al. et studies previous where between at500mrichness values those 1000m at and wereintermediate evident at1000 explanationmprecipitation, is nosuchsimpleenvironmental with and contrasts 2011). formed species of bythree associatedwithare richness m, wasfound lowfern and3500 richness whereforests at3000m 37-63% in disturbed in secondary forests (DF)37-63% and (SF) natural to (NF) compared forest At Human impact et 2014).composition al. (Carvajal-Hernández and regions,floristic physiographic with different environments, substrates, windexposure, However, the filmy familyHymenophyllaceae fern such epiphytessome of as species, from individuals temperaturesof high fatal that can be for the temperature (Kessler 2001b (Kessler elevational of turnover species difference ofm, 200 with 20% which typically goes along about at NF anbetween mis similar 1500 andDF/SF recorded to may tobeminor,appear it temperature Bader2009). Although & the al. difference ofabout Zotz (Scatena et 2005; 1°C and temperature intensity relative conditions and lower airhumidity forests non-natural (RH) in major to withhighrelated changes structure light inforest and accordinglymicroclimate, in NF other. and between the andSFon ontheonehand This was DF species turnover of50-70% al.2014). recorded Atthese et wealso elevations, 70% relative high toNF (Carvajal-Hernández foreststheinmontane withinplantations study humid region, fern richness even is reduced by

Acceptedm,m,m,m, of and2500 2000 species richness 500 ferns wassignificantlyreduced by 1500 Article Yet, while low Yet, while diversitycan berelatedto and elevations atthese lowtemperatures

, wa at se this some forests elevation documented with studies ). s 7°C werenot in present because are partconsidered study the they ofdifferent

It should be noted that the fluctuation between maximum the shouldbenotedthatthe minimumIt and in SF. This difference means day SF.Thisthroughout the difference that periods short there are Pinus Quercus andoneof . The majority of the individuals ofthisThe majority ofthe individuals family disappeared (C.I. Carvajal, obs.A similar pers.). situation (C.I.Carvajal, of lowtree Abies (Ávila-Bello 2011; Castillo-Campos et al Castillo-Camposet (Ávila-Bello 2011; at this elevation, this diversity a higherdiversity of ferns. . In tree . ( forests.ofmontane This filmyalmosthumid NFin included to species epiphytic restricted ferns disturbance, is the of individualsthe the loss stronger thatgreater species. the of who report their smallefficienttheir fronds thedwarfismbecause light conditions, tendencies combined hygrophilous biology, witha as highairhumidity survival known torequire undere.g., are low fortheir beabletothrive and to (Dryopteridaceae) (Carvajal-Hernández al.2014). et (Dryopteridaceae) susceptible to includedthe disturbance filmyferns andthe genusterrestrial a previous study incentral Veracruz were taxacomparing that especially NFwithagroforests, on their the fernsto tolerate vitariod changes inthe no ability studies there are specific habitat. of In thecase (RiañoBriones, gametophytic & 2015). the (as to wetenvironments in NF) phase Scoliosorus Scoliosorus ensiformis (Polypodiaceae) such ferns as for some species. This findings withthe is Carvajal-Hernandez of in accordance for some et species. to related the fluctuation intemperature, record ofthelowest asituation that may bebeneficial disappearprimary amore fernsthat whenthereis changeabrupt habitat. inthe is This probably ofthelow number inspite ofspecies aninteresting Therefore, represents DF,reservoir of in it primary other species that inturn the do mostnot resist climatic contrasting conditions of SF. conditions thatthe DF at isaccentuated between andSF medium 3). lowelevations (Fig. Thisindicates and torichnes relative species statistically of turnover the SF. However, terms diversity, in ofbeta of changesby areparticularlysusceptible high cover epiphytes tostructural human disturbance. humidforests, Itthusappears montane types. that which haveadense,evergreen canopy and 2003; Saldaña etal.2014)2003; (filmy andgrammi beenpreviously identified particularly sensitiveto changes asbeing microclimatic in conditions as This article isThis article by protected copyright. All rights reserved. humidity reduced byabout conditions 20%, (Carvajal-Hernández Krömer,& areas Combined subject disturbance in the to 2015). withair Didymoglossum tegularis reptans, Hymenophyllum

AcceptedAlsophila firma Article The indicator species analysis indicator analysis The species recovered highest the restricted number or ofspecies It should be noted that the DF retains less species richness than NF but does not differ doesnot bebut should that theDF richness lessspecies thanNFIt retains noted of the DF affect some very sensitive species the NF. conservesthe some However, DF species DF still sensitive the affect very (Cyatheaceae)and tid fern groups) (Gehrig-DownieFilmy al. et ferngroups) 2013; Krömer ferns, 2013). etal. and . ly In the Inthe case of Vittaria gramminifolia absorb filmy al. bydiffusionet water on their (Dubuisson lamina Terpsichore asplenifolia Marattia laxa Marattia Alsophila firma Alsophila we re quiteclearly different distinct forest in the , as well assome species, aswell such terrestrial large (Marattiaceae) , and , and vittarioid (Pteridaceae) suchas ferns , a specialization, a demonstrated hasbeen Polyphlebium capillaceum . Several oftheseferns have Phanerophlebia al ), grammitid), . (2014),

In zone of the elevational morezone ofthe elevational In contrast, in the humidgradientmountain forests arefound. where specially conservation ofspecies, is considered the in intermediate animportant habitatfor the beta considering the diversitydiffer however, strongly from ofNF; theDF among those habitats, elevational this beltare only oflimited because conservation value their microclimatic conditions human DF typewithout andSFin of vegetation In terms richness, this intervention. of species montanein the ofhumid forests fragmentsflora region, study isimportant it topreserve natural implications forfern management tropical forest conservation. Toadequatelypreserve the and thoseof (Wernerthan 2011).Our forests potential 2005; et haveimportant cloud findings al. Andes, whereepiphytic assemblagesofdry areplant impacted forests less byhuman disturbance areless they has been disturbance.documented affected Asimilar byforest the in situation byinhabited fern species insolation.Accordingly, humidity high already adaptedto air and low ofcontrast, theends thegradient open are dry naturally andcomparatively forests atthe BaderIn & 2009)oramphibians 2002). 2009; (Vallan bryophytes (Spornetal. such as Zotz depend Thesame flora. groupsthat onhigh other assumedairfor may be oforganisms humidity Carvajal-Hernández(Larrea 2010; &Werner fern etal. that stronglyaffect the conditions 2014) so that transformation changesgreat in structurethe microclimatic oftheforest leads to tobe affectedappear because naturally strongly of their highhumidity and low light availability, inthestudyHumidforests susceptible montane to region human to degrees. varying disturbances and conditions thus are less affected by human disturbance. of studyends the species surviving at are already transect environmental the adapted to stressful limitingwater, suitability their forepiphytes (Callaway et al. fern2002). Forthesereasons, Wesenbeeck 2003) etal. thin and their branches with unstable barkthat does absorb much not (van needles forunsuitable becauseof ferns their litter ofslowly dense layer decaying vegetationpines, structure isalsoquite open.In addition, pine appear tobegenerally forests dominatedare by similar by used humans.conditions toforests elevations, forests Athigh where forests offers microclimaticthese atleast are deciduous,sothateven NFseasonally partly that mayWe 20-30%. pronounced this consider tothefact at berelated that atlowelevations Accordingly, indisturbed forests. richness species turnover betweenNFandDF/SF less was This article isThis article by protected copyright. All rights reserved. Accepted ArticleSF was less 10%, was less around pronounced onoccasionat and weevenrecorded highe slightly Concluding, shows the ourstudy fernassemblages that ofdifferent forest typesare At the ends of the gradient (20 m, 1000 m, 3000 m, and 3500 m), species loss in DFand m,ends m), (20m, of m, and3500 gradient At the loss the 1000 3000 species r This article isThis article by protected copyright. All rights reserved. byKrömer wassupported CONACy provided a (No.224291)to the (CONACyT) PhD scholarship author. The researchfirst ofT. CienciayTecnología ConsejoNacional enMéxico de former also with map.helped The the and Valeria for fieldwork, Guzmán-Jacob, help during We the Samaria thank Armenta-Montero Acknowledgements the highest priority. withouthumanreserves clearlyhave use should instrict conservation their Neotropics, forests that cloud ofthecan befound parts inlarge toconfirmneeded ofour generality the conclusions, considering lowthe but coverofnatural fo forest managementextensive strategy appropriate survival isan to ensure the ofmuchof the maintained, themicroclimatic conditionsare similar to those of NF. asituation, the Insuch conservation oftheassociated of ends the open forests thegradient,at human partly isat least compatible use with the Science stomatal T.J. of Brodribb, Passive origins control &McAdam, vascular A.M. 2011. in plants. patterns in neotropical dry in patterns forests and conservation their implications. M.,Quintana,Prado, D.,Pullan, C., R., (…)Riina, Pennington,R.T. & 2016. K.G., A.,R., Oliveira-Filho, Delgado-Salinas, Banda, R.K., Dexter, Linares-Palomino, A., AC, México. Biodiversidad, Gobierno de del Estado Instituto de Veracruz, Ecología Universidad Veracruzana, Estudio deEstadoVeracruz: deoyamel bosques Ávila-Bello, C. 2011. Los ( References

Accepted Articleof biota. be rest fromAdditional studies organismswill regionsandfor other other groups 331: 581-585. , pp. 181-194. Comisión, pp.181-194. Nacional paraelConocimiento yUsodela fe rn flora, because as long as a forest-like vegetationflora,rn structure because asaforest-like is aslong T.

Abies ). In: Conabio). In: (ed.) Science Labiodiversidad en Plant diversity 353: 1383-1387. 353: Castillo-Campos. S. G., Avendaño-Reyes, Veracruz, México. Veracruz, de montaña de enbosquemesófilo florística pteridobiontes en de centro yambientesel asociados 2014. C., M. RiquezaCarvajal-Hernández, Vázquez-Torres, Krömer, T. ycomposición & 93:601-614. quantitative quantitative review. Wright, 2009.Thefuture oftropical S.J. & insecondaryforests: D.H.Dent, species A intropical yields agroforests. D.,Cicuzza, K., Darras, (…) A., D., Wanger, Buchori, T.C., M., Anshary, Y., Kessler, J., Clough, Juhrbandt, Barkmann, J., de Instituto Veracruzana, AC, Ecología México. elConocimientopara Biodiversidad, yUsodela del de Gobierno Estado Veracruz, Universidad This article isThis article by protected copyright. All rights reserved. Conabio (ed.) preferenceshost interactions. andhost traits: mechanismsspecies-specific for K.O., R.M., G.W., D.J. Reinhart, &S.C. Moore, 2002.Epiphyte Pennings, Callaway, Moore, gradiente altitudinal del Cofre de Perote, centro de Veracruz, altitudinalgradiente delMéxico. centro deCofre dePerote, Veracruz, C. Carvajal-Hernández, Krömer,T. 2015.Riquezaydistribución& dehelechos y el licófitos en 132:221-230. fl Legendre, assemblages P. & 1997.Species M. Dufrêne, and indicator species: theneed fora in H. 2003. Schneider, diversity S., Ecological J.Y., Rakotondrainibe, Hennequin, F. & Dubuisson,

exible asymmetricalexible approach.

AcceptedTrichomanes Article La biodiversidad enVeracruz: Estudio Estado, de (Hymenophyllaceae). Revista Mexicana Revista Mexicana Biodiversidadde BiologicalCons &Tscharntke, T. 2011.Combining highbiodiversity with high Proceedings of Sciences the National Academy of Ecological Monographs erv Botanical JournalBotanical of SocietyLinnean the ation & 142:2833-2843. Medina-Abreo, yvegetación. In: 2011.Flora M. 85:491-501. 67:345-366. pp 163-179. Comisión pp163-179. Nacional Botanical SciencesBotanical Oecologia 142:41-63. 108:8311-8316.

groups inthe Bolivian Andes groups central M. species and gradientsin 2000. Elevational richness plant endemismKessler, of selected CDClimatológica ERICII. Mexico. ROM. Rápido Extractor (Instituto Información MexicanoIMTA deTecnología delAgua) de .2000. 41:520-529. diversityepiphyte inshade plantations cacao inthe ChocóRegionofEcuador. H.de 2009.ConservationofHaro-Carrión, T.,& X., Navarrete, Koning C.H.J. Lozada, vascular disturbanceinBolivianmontaneanthropogenic forests. M. 2001b. MaximumKessler, community plant endemismintermediate of at intensities transect intheelevational Andes. Bolivian M. ofdiversityand Patterns 2001a. range ofselected Kessler, size plantgroupsalong an irreplaceable for sustaining tropical biodiversity irreplaceable for tropical sustaining J.A.,W.F., areBradshaw, Laurance, forests T.E.& Lovejoy, Sodhi,N.S.2011.Primary T.A., L.T.,Pin,K.L., B.W.,Gibson, L.,Ming, Gardner, Brook, C.A., Barlow, J.,Peres, epiphytes. epiphytes. A.H. and vascularDiversity Dodson, of C.H. & biogeography Gentry, 1987. Neotropical This article isThis article by protected copyright. All rights reserved. Accepted Article forest”. cloud distributionvertical offilmy foridentifying the atool nd fernsas type“tropicallowla novelforest Obregón, S.R. J., & C., J. A., and Marquardt, Gradstein Bendix, 2012.Diversity Gehrig-Downie, EcologyPlant &Diversity humanEinzmann,H.J., Döcke,G. 2016.Epiphytes in L.&Zotz, in rural settlements Panama. Annals ofthe BotanicalAnnals GardenMissouri Ecotropica 18:35-44. 9:277-287. . Plant EcologyPlant Biodiversity andConservation Biodiversity . Nature Nature 74:205-233. 149:181-193. Conservation Biology 478:378-381. 10:1897-1921. 15:634-641. Biotropica

pteridophyte records for the State of Veracruz, Mexico. for Stateofpteridophyte records the Veracruz, C., T., Carvajal-Hernández, Krömer, A decadeofnew A.R. A.R.Smith, Acebey, & 2015. 82:29-44. State, inVeracruz Mexico. ofgrammitid Polypodiopsida) status ferns(Polypodiaceae, A.R. T., Acebey, Taxonomic distribution Krömer, A.R. Smith, update, and & 2013. conservation effects diversity. onglobalpteridophyte seed plant and W., Barthlott, W. & Kreft, H., Jetz, M. environmental Mutke, Contrasting 2010. andregional This article isThis article by protected copyright. All rights reserved. Andes. communities bird and alongtwogradients ofelevation, humidityBolivian and land the usein J. M.,& S., richness Fjeldsa, Bach,C. Herzog, Species and 2001. endemismKessler, plant of Neotropical forests. M. groups Bach,K. 1999.Usingindicator & for classificationKessler, inspecies-rich vegetation Accepted Animal Ecology of Journal LennonJ.J. beta K.J. & 2003.Measuring Koleff,Gaston, forP.,diversity presence gradient in Costa Rica. geometric constraints, climate on pool anelevational forpteridophytes effects andspecies What & elevational M. Kessler, Dunn, patterns drives Atest J., R.Kluge, of diversity? 2006. of Article 102:1623-1633. regional andlocalscales. at relationships of ferns terrestrial tropical J. Kluge, M., Speciesrichness-productivity & 2014. J. L., Homeier, Salazar, Kessler, species richnesspatterns elevational of ferns. M., comparative Hemp, J., Kluge, global analysis R.A. Ohlemüller, A of Kessler, 2011. & Diversity and Distributions and Diversity Phytocoenologia Global Ecology BiogeographyGlobal and 72:367 – 7:61-77. 382. 29:485-502. Global Ecology Ecology and BiogeographyGlobal Ecography Am 15:358-371. erican FernJournal 33:408-419. Journal of EcologyJournal of 105: 162-175. 105: 20:868-880. – absence data. Phytotaxa

andPalynology Paleobotany strategiesin C. 2002.Ecological Page, aneopteridological fernevolution: overview. a tropical Brazil.a tropical rain forest in 2005.Effects J. fragmentationPaciencia, M.L.B. Prado, offorest & onpteridophytediversity in España.Zaragoza, C.E. para medir 2001.Métodos biodiversidad. Moreno, la CYTED, ORCYT/UNESCO &SEA. and Biology of evolution andlycophytesferns Haufler, T.R. biogeography, & In: 2008.Diversity, C.Ranker, andfloristics. (eds. Moran, Botanical Gard Botanical & J. 2004. Thepteridophytes Smith Mickel, A.R. of Mexico. Nacional México. Instituto Ecología Instituto AC, 83-93. de deEcología, K. (eds. V., S. Gallina, & Mehltreter, R., In: Hernández-Ortiz, K.Mehltreter, 2008.Helechos. Manson, This article isThis article by protected copyright. All rights reserved. Accepted Article inaneotropicalintensities montane wetforest. Werner, differentResponse ofvascularM.R. epiphyte & to diversity F.A.Larrea, land-use 2010. gradient alongepiphytes the anelevational in Andes. Diversity M., ofvascularA.R. S.R.patterns Acebey, Gradstein, 2005. & T., Kessler, Krömer, Ecology submontane ofthe Andes: andmontane forest the Bolivian of importance understory. the M. stratification Gradstein,Vertical of epiphytesin & S.R. T., Kessler, vascular Krömer, 2007. ) 189:261-278. Agroecosistemas deVeracruz:biodiversidad, manejo cafetaleros yconservación, en 88:1-1054. 119:1-33. Plant Plant Ecology 180:87-104. , pp Cambridge U.K. 367-394. Press, For est Journal ofBiogeographyJournal Ecology Management and Memoirs of theNewMemoirs York 32:1799-1809. 260:1950-1955. Review of Plant Plant ) pp This article isThis article by protected copyright. All rights reserved. Kröm M., M.,S., Lehnert, Abrahamczyk, Kessler, L., J., Homeier, Salazar, Botánica de de Sociedad Boletin la México derivadasecundaria deselvahúmeda montaña de Cruz deSanta Tepetotutla, (Oaxaca), México. florístico S., Análisis J. Castillo, Romero, M., vander delavegetación H. Meave, & Wal, 2000. Tropical Biología ambiental enelbosque templado deSanJerónimo Amanalco, Texcoco,México. Pacheco M.L., Rodríguez-Romero, Zavala, 2008. Pteridofitas H.J. L. & indicadoras de alteración Botany of variation radiationsolar andwateravailability Mexican ina forest. cloud O.2015.Sensivityofthree Briones, Riaño, K.& first ferns during phaseoflifetothe their Accepted Uso delaBiodiversidad, México. diversidad, México: ymanejo, ecología Gual-Díaz, Rendón-Correa, amenazado. In: & M. A. (comps.). G. demontaña:Sánchez-Ramos, R. 2014.Elbosquemesófilo unecosistema &Dirzo, prioritario Biodiversidad, México. Comisión dela Nacionalpara Conocimientoel yUso de Estadode vol.Natural México, II: conservación cambio, ytendencias de por causashumanas. ecosistemas Conabiotransformación delos In: (ed.) terrestres S., & I.A. Flores-Martínez, Sánchez-Colón, Velázquez, A. y A., 2009.Estado Cruz-Leyva, fern species temperatein a rainforest. successional forest status onmicroenvironmental and conditions,diversity, distribution of filmy A., Bravo, M.J., L.J.Effects & A.,Corcuera Flores-Bavestrello L.A. Parra, of 2014. Saldaña, Diversity patterns2015. Diversity in forests.of elevation Andeantropical ferns along Article 102:1472-1481 8:13-24. 56:641-656. Plant SpeciesPlant Biology pp 109-137. Comisión elConocimiento Nacional y para 67:89-106. 67:89-106. 29:253-262. Bosques mesófilos de montaña de demontaña Bosques mesófilos er pp 75-129. pp75-129. Plant Ecology & Plant American of Journal , T. & Kluge, J. J. Kluge, , T. & Revista de Capital Capital rain forests rain Madagascar. of eastern environmentalD. diversity onamphibian 2002.Effects in ofthe Vallan, changes anthropogenic Defining beta diversity Defining betadiversity as afunction andof alpha gamma diversity. of H. diversities: 2010.Adiversity Tuomisto, beta straightening upaconceptgoneawry. 1. Part Zapata,Emiliano Veracruz, México Torres-Cantú, G. 2013. elConocimiento Biodiversidad, para México. yUsodela de y manejo diversidad,ecología mesófilos montañadeMéxico, This article isThis article by protected copyright. All rights reserved. of forests. Bruijnzeel, L.A. Bonell, humidhydrology In: tropical M. & F.N., E.O. 2005. J. Scatena, Planos-Gutierrez, Natural Schellekens, disturbances andthe & tropical ferns is evolutionarily linked to water transport capacity. fernstropical evolutionarily linked is transportcapacity. towater Z.,Sun,M.,Kun-Fang, C.,Hong of Z.2014.LeafphotosyntheticShi-Bao, rate H.&Jiao-Lin in thepeople humidtropics, mesófilo de montaña en México. In: Gual-Díaz, M. & Rendón-Correa, A.In: Rendón-Correa, (eds. mesófilo & Gual-Díaz, M. demontañaen México. yhelechos Licopodios 2014. en elbosque M. A.Gual-Díaz, & D.,Tejero-Díez, Torres-Díaz, 179. agroforests of and cacao bryophytes rainforest in Indonesia. Microclimate determines community richness composition butnot ofepiphytic understory S.R. Gradstein, & M. Kessler, 2009. M., S.G., Hoffstätter-Müncheberg, Sporn, Bos, M.M., AC Veracruz, Biodiversidad, Gobierno de del Estado InstitutoUniversidad Veracruzana, de Ecología Estudio deEstadoVeracruz: Accepted Article Conabio Giddings, B.L. & M. (ed. 2011.Clima. In: Soto-Esparza, doi:10.1371/journal.pone.0084682. , México. , México. Lista Floristica de la Barranca Floristica de la Monte Obscuro,Lista de municipio de pp 489-512. Cambridge University Press, USA. pp489-512. Cambridge Press,USA. University , pp35-52. para Comisión elConocimiento Nacional yUsodela Journal of Tropical EcologyTropical Journal of . México. Thesis, deMaster Colegio Posgraduados, Functional Biology Plant Functional 18:725-742. , pp199-220. Comisión Nacional Plos One ) La biodiversidad en Ecography (e ds. 9:e84682 9:e84682 ) Forest, Forest, water and 33:2-22. ) Bosques 36:171- This article isThis article by protected copyright. All rights reserved. ferns along gradientan elevational in CostaRica. J.E., richnessanddistribution of Watkins, R. Moran, Species Cardelús, R.C., 2006a. & Colwell, Conservation Biological of aplantation with Wesenbeck, B.K. J.F.Van effects Cleef, VanMourik, A.M. T., 2003.Strong & Duivenvoorden, forest. forest. T.C., Brown, R. speciesWhitmore, in & K. Peralta, 1985.Total count a Costa Rican tropical rain Monographs Vegetation R.H.mountains,Whittaker, of Siskiyou 1960. the Oregonand California. assemblages human of to climate? local afunction disturbance the M. Is ofepiphyte Gradstein,resilience N., & S.R. F.A., Kessler, 2011. Köster, Werner, remnant montane inthe forestbelt trees ofsouthernEcuador. Gradstein,F.A., & S.R. J. Homeier, Werner, on 2005.Diversity epiphytes ofisolated vascular 92. photoinhibitionagainst protect fromscales laminar excesslight. J.E.,Watkins, K.2006b. S.A.,Auld Kawahara,A.Y.,Leicht, Bicksler A.J.,&Kaiser J.R., Fern Accepted and vascular 70:147-170. non-vascularProgress epiphytes. in Botany plants effects G. & M.Y. inachangingZotz, 2009.Epiphytic Bader, global change world: on Article Journal of TropicalJournal of Ecology 30:279-338. Pinus patula 114:207-218. on Andeansubparamo a vegetation: case studyfrom Colombia. 1:375-378. Am erican Journal of Botany Journal of erican Ecotropica Ecotropica American FernJournal 11:21-40. 17:15-20. 93:73-83. Ecological 96:83- This article isThis article by protected copyright. All rights reserved. transmissionLight Temperature (ºC) intensity (lux) Light (%) Relative air humidity disturb Table 1 Accepted Article Mexico. Veracruz,

ed Correlation matrix of climatic variables in the three different habitats habitats (natural matrix ofclimaticforest, Correlation variablesinthethreedifferent forest and forest along secondary forest) at the elevational Cofregradient dePerote, (%)

0.77 -0.14 0.45 -0.24 (%) openness Canopy -0.34 -0.34 0.300 -0.38 humidity (%) humidity (%) Relative air 0.50 -0.13 intensity (lux) Light -0.22 -0.22 Temperature (ºC) This article isThis article by protected copyright. All rights reserved. Accepted silvestris stellata Selaginella Scoliosorus ensiformis orizabae Pteris Pteridium aquilinum Polypodium puberulum Polypodium conterminans Polyphlebium capillaceum polylepis Pleopeltis sursumcurrensPecluma laxaMarattia Lophosoria quadripinnata tegularis Hymenophyllum Elaphoglossum vestitum Elaphoglossum sartorii Didymoglossum reptans striatum Diplazium franconis Diplazium Article sellowiana Dicksonia fragilis Cystopteris Campyloneurum phyllitidis Campyloneurum amphostenon wardiae Blechnum falciformeBlechnum harpeodesAsplenium Alsophila firma andicola Adiantum Species recorded type, forest ranging from in recorded). type)to that 1(only forest 0(not DF:disturbed valuesreflectforest; affinity forest; SF:secondary forest. specific*IndVal toa Table 2 Indicator species of the three forest types recovered in the IndVal analyses. NF: species Indicator analyses. natural types ofthethree forest intheIndVal recovered

2500 2000 2000 1500 1500 1500/2000 1500/2000 1500 2500 1500 1500/2000 2500 2000 1500 1500 1500/2000 2000 2000 2000 3000 500 2000 2000 2000 1500/2000 1500 500 (m) Elevation NF NF NF NF SF NF NF NF type Forest SF NF NF DF SF SF NF NF NF SF NF DF NF NF NF NF NF NF NF

0.476 0.812 0.7 0.8 0.692 0.75/0.75 0.857 1 IndVal* 1 1 0.8 0.8 0.8 0.800/0.588 0.746/0.642 0.75 0.777 0.592 0.800/0.558 0.515 0.8 0.833 1 0.8/0.8 0.8 0.647 0.9 0.028 0.003 0.032 0.01 0.017 0.018/0.007 0.004 0.002 p 0.002 0.003 0.008 0.014 0.011 0.012/0.049 0.010/0.015 0.002 0.004 0.041 0.017/0.016 0.006 0.015 0.003 0.002 0.012/0.009 0.006 0.025 0.002 This article isThis article by protected copyright. All rights reserved. Accepted Article Vittaria gramminifolia Thelypteris rudis Thelypteris dentata Terpsichore asplenifolia heracleifoliaTectaria 1500/2000 1500/2000 1500/2000 1500 1500 500 NF SF DF NF NF

1.000/0.628 1.000/0.628 0.666/0.823 0.6 0.8 0.947 0.003/0.029 0.003/0.029 0.002/0.002 0.049 0.01 0.004