secondary succession under invasive species ... · howtocitethisarticlejean baptiste a, macario pa,...

Submitted 2 March 2019Accepted 15 April 2019Published 28 May 2019

Corresponding authorJorge O Loacutepez-Martiacutenezjorgelopezecosurmxlmjorgeomargmailcom

Academic editorTatiana Tatarinova

Additional Information andDeclarations can be found onpage 10

DOI 107717peerj6974

Copyright2019 Jean Baptiste et al

Distributed underCreative Commons CC-BY 40

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Secondary Succession under invasivespecies (Pteridium aquilinum) conditionsin a seasonal dry tropical forest insoutheastern MexicoAlberto Jean Baptiste1 Pedro A Macario1 Gerald A Islebe2 BenedictoVargas-Larreta3 Luciano Pool4 Mirna Valdez-Hernaacutendez2 and Jorge O Loacutepez-Martiacutenez15

1Departamento de Agricultura Sociedad y Ambiente El Colegio de la Frontera Sur Chetumal Quintana RooMexico

2Departamento de Conservacioacuten de la Biodiversidad Herbarium El Colegio de la Frontera Sur ChetumalQuintana Roo Mexico

3Divisioacuten de Estudios de Postgrado e Investigacioacuten Instituto Tecnoloacutegico de El Salto El Salto DurangoMexico

4Departamento de Agricultura Sociedad y Ambiente El Colegio de la Frontera Sur Campeche CampecheMexico

5Caacutetedras CONACYT Ciudad de Meacutexico Mexico

ABSTRACTThe role of invasive species in ecosystem functioning represents one of the mainchallenges in ecology Pteridium aquilinum is a successful cosmopolitan invasive specieswith negative effects on the ecological mechanisms that allow secondary succession Inthis study we evaluated the influence of P aquilinumon secondary succession underdifferent disturbances in a seasonal dry forest of the Yucataacuten Peninsula We determinedspecies richness composition and the relative importance value in four sampling unitsFabaceae followed by Asteraceae Meliaceae Rubiaceae Sapindaceae and Verbenaceaewere the most species rich families A dissimilarity analysis determined significantdifferences in beta diversity between sampling unitsWith a generalized linearmodel wefound that species richness was best explained by site conditions followed by calciumand soil organic matter Also the generalized linear model showed that abundanceresulted in a strong correlation with site conditions and soil characteristics Specificsoil conditions related to phosphoro and calcium were also detected as beneficiary tothe successional processes Our results suggest that applying fire restriction and periodiccutting of the bracken fern this can increase a higher diversity of species

Subjects Biodiversity Conservation Biology Ecology Plant ScienceKeywords Yucataacuten Peninsula Secondary succession Bracken fern Fire Invasive species

INTRODUCTIONPteridium aquilinum (L) Kuhn is considered one of the most successful global invasivespecies Its distribution is related to processes of land use change derived from humanactivities eg agricultural and livestock activities (Rymer 1976) This species is particularlysuccessful when light is not a limiting resource (MacDougall amp Turkington 2005 Schneider2006) P aquilinum allelopathic characteristics and their tolerance to a wide range of

How to cite this article Jean Baptiste A Macario PA Islebe GA Vargas-Larreta B Pool L Valdez-Hernaacutendez M Loacutepez-Martiacutenez JO2019 Secondary Succession under invasive species (Pteridium aquilinum) conditions in a seasonal dry tropical forest in southeastern MexicoPeerJ 7e6974 httpdoiorg107717peerj6974

environmental and soil conditions have helped to colonize almost all terrestrial ecosystemsexcept for deserts (Gliessman 1976 Taylor 1989) They have an underground rhizomewhich branches into long and short buds can grow up to 2 m in a single season whichgives it a great capacity for colonization (Fletcher amp Kirkwood 1979) Additionally throughthe creation of a physical barrier generated by the density of its canopy it hinders theestablishment of native species (Olson amp Wallander 2002) Similarly it has been observedthat the accumulation of biomass from the dry fronds modifies the frequency and intensityof fires due to the increase of available fuel (Frankland 1976 Crane 1990) This exhauststhe seed bank and limits the growth of seedlings (Da Silva Matos SR da de 2006) Thelack of competitors for limiting resources (Vandermeer 1972) the absence of pests andherbivory and their resistance to fire due to their ability to regrow from their rhizomesgive them strategic advantages over native species (Tolhurst amp Turvey 1992) Studies fromBrazil Ecuador the Dominican Republic and Rwanda found that former active agriculturalregions are currently held back due to the interruption of secondary succession processes(Hartig amp Beck 2003Gallegos et al 2015) InMexico most of the studies have been carriedout in the south mainly in the states of Quintana Roo Campeche and Oaxaca (Schneider2006 Suazo-Ortuntildeo et al 2014) Likewise it has been observed that the lack of strategiesfor their control can generate a substantial growth in a relatively short time eg Schneideramp Fernando (2010) found in the Calakmul reserve that their coverage increased from 40km2 to 80 km2 between 1982 and 2010 It was also observed that landscapes with invadedareas are less productive have a reduced biological diversity and show severe impacts inthe socio-economic dynamics of the affected regions because the areas cannot be usedby the owners (Schneider 2004 Schneider 2006 Suazo-Ortuntildeo et al 2014) Currentlyinsufficient studies have been developed in seasonally dry tropical forests that provideinformation on the historical effect and management of areas invaded by P aquilinumand its impact on the richness and floristic composition and their influence on successionStrategies are needed to restore areas affected by one of the most important invasive speciesin the world It is important to mention that the establishment of invasive species affectsthe possibility of maintaining the net primary production of the ecosystems (Ewel amp Putz2004 Gibbons et al 2017 Feng Fouqueray amp Van Kleunen 2019) Consequently the aimof this work was to determine the effect of the invasion of P aquilinum on secondarysuccession in a seasonally dry tropical forest

MATERIALS amp METHODSStudy siteThe study was carried out in the ejido (communally managed land) Laguna Om (minus8915W1870Nminus8887W 1840NWGS 84) in the south of the state of Quintana Roo Mexico withan area of 84998 ha (Fig 1) The ejido is located in the geological formation called Peteacutenwhich belongs to the Paleocene-Eocene and is characterized by massive compact macroand microcrystalline limestones which have yellow to white coloring with brown partsstained by iron oxides (Wright 1967 INEGI 1993) The terrain is flat with an undulatedmicrorelief and with wide depressions that present small plains Its altitude above sea levelvaries between 100 and 150 m (Garciacutea 1997 INEGI 1993 IUSS Working Group WRB

Jean Baptiste et al (2019) PeerJ DOI 107717peerj6974 216

Figure 1 Study site Location of the four sampled sites and information on vegetation types and coveruse

Full-size DOI 107717peerj6974fig-1

2015) The climate is Aw (xrsquo) i warm subhumid with precipitation in summer and some inthe winter (Garciacutea 1997) The climatological station located in the center-south part of theejido reports 1290 mmyear of precipitation and an average annual temperature of 26 CSoils are Leptosols Vertisols and Gleysols (INEGI 1993) The dominant vegetation in thestudy area is seasonal dry tropical forest and the terrain is low seasonal flooded forest andsavanna (Miranda amp Hernaacutendez 1963)

Sampling designSampling units were selected based on several conditions Each of the four sampling unitshas eight plots (SU) of 10 times10 m (100 m2) which were randomly selected This gives atotal of 32 plots To evaluate the importance of the soil properties on the richness andabundance of species soil samples were taken in all the sampling units 12 soil samples perplot were mixed giving one composite sample of 2 kg for each sampling unit Soil analyseswere based on the Official Mexican Standard (NOM) 021 RECNAT-2000 The soil sampleswere dried at room temperature (22ndash25 C) macerated and sieved with a 10 mm meshscreen and the following characteristics were analyzed Total nitrogen (Nt Micro Kjeldahlmethod) Phosphorus (Olsen method) Potassium (K AS-12 with ammonium acetate)pH (Walkley and Black method) texture (Bouyoucos method) Ca Na and soil organicmatter (SOM)


Plots characteristicsThree sampling units were established in areas invaded by P aquilinum for approximately50 years (from 1960 till present) The age and the frequency of fires of the sample unitswere defined according to the information provided by local farmers Sampling unit 1(SU1) consisted of areas with regular periods of burning every two or three years duringthe last fifty years The last recorded fire occurred in 2015 vegetation sampling was carriedout one year after the last fire (2016) Sampling unit 2 (SU2) was established in areasinvaded by ferns during the last 50 years but the last burning occurred 12 years ago(2007) In SU1 and SU2 fires were natural and the presence of abundant biomass ofP aquilinum and together with higher temperatures during the dry season increased fireprobability Contrary sampling unit 3 (SU3) was established in areas with a similar landuse history but since 2010 fire was controlled and the removal method applied byMacario(2010) was applied This method consists of weekly cuttings (locally known as chapeos)during two months followed by monthly cuttings throughout the year Later quarterly andsemi-annual cuttings are applied depending on the density of the fern A fourth samplingunit (SU4) was established in areas that were burned for the last time in 2007 for theestablishment of the milpa system (slash-and-burn agriculture) and was left for recoverysince 2009 This area never presented invasion by ferns All the sampling units presentedsimilar conditions in relation to climate stoniness slope and altitude

SamplingThe sampling was carried out betweenMay and June 2016 In each of the plots the followingvariables were recorded diameter at breast height (DBH) of all tree species gt05 cm andthe taxonomic identity of each species (Wyatt-Smith amp Foenander 1962) All registeredindividuals were identified from dichotomous botanical keys (Standley amp Steyermark1958) and existing floristic listings (Sousa amp Cabrera 1983 Pennington amp Sarukhaacuten 2005)The community of plant species was characterized in each of the four SUs establishingrichness and abundance The Importance Value Index (IVI) was determined in each of thetreatments

IVI = relative density+ relative basal area+ relative frequency

Where relative density = (number of individuals of speciestotal number ofindividuals)100 relative basal area= (basal area of a speciesbasal area of all species)100relative frequency = (frequency of a species frequency of all species)100 (Kent 2011)

Data analysisTo compare the taxonomic diversity of the treatments a rarefaction analysis (interpolation)and extrapolation (prediction) of the Hill numbers were performed based on sample sizeand coverage which represents a unified criterion to contrast the diversity of multipleassemblages (Hsieh Ma amp Chao 2016) The analysis was carried out based on the order q(richness of species) and richness estimators were determined with the iNEXT softwarepackage R (Chambers 2008 Hsieh Ma amp Chao 2016) The variation in the compositionof species was analyzed through a non-metric multidimensional scaling (NMDS) Toreduce the effect of very abundant species and to level the effect of rare species the fourth


Table 1 Sampling units characteristics with richness of taxa abundances of shrubs trees and Pterid-ium All abundances were calculated with areas of 100 m2 Fire frequency is expressed as decadal eventsfor the last 50 years

SU Family Genus Species Shrubsabundances

Treesabundances

Totalabundances

Fronds ofP aquilinum

Decadal firefrequency

SU1 9 10 11 0 193 193 3500ndash4000 15SU2 13 18 20 13 57 70 800ndash1100 10SU3 20 31 34 56 752 808 0 10SU4 32 49 54 209 882 1091 0 12Total 33 56 63 278 1884 2162

root transformation in the PRIMER-E 6112 software was applied Statistically significantdifferences in the composition of tree species between the different plots were calculatedwith a dissimilarity analysis (ANOSIM) in PRIMER-E 6112 (Clarke amp Gorley 2006)Finally a generalized linear model (GLM) was carried out between the species richness andabundance and the soil variables with the package glm2 (Marschner 2011) in the R software(R Development Core Team 2012) Prior to the analysis multicollinearity of variables wasestablished to avoid redundancy (Zuur Hilbe amp Ieno 2013)

RESULTSComposition and floristic richnessThere were 2162 individuals belonging to 33 families 56 genera and 63 species recordedin the 32 sampled plots (SU1 to SU4) Of the total recorded individuals 1884 (87)were trees and 278 (13) shrubs The sampling unit with the highest diversity was SU4with 32 families 49 genera 54 species and 1091 individuals of which 882 were trees and209 shrubs On the other hand SU1 showed the lowest species richness with 11 speciesbelonging to nine families and a total of 193 trees without the presence of shrubs (Table1) The families with a higher richness of recorded species were Fabaceae with 11 speciesfollowed by Asteraceae Meliaceae Rubiaceae Sapindaceae and Verbenaceae with threespecies each contributing 41 of the total of the species registered in the plots The generathat presented the highest number of species were Lonchocarpus with five and ThevetiaEugenia and Coccoloba with two species respectively The largest number of individualswas distributed among the following families Rubiaceae with 572 Araliaceae (237)Fabaceae (233) Polygonaceae (159) Cecropiaceae (134) Asteraceae (115) Ulmaceae(110) and Sapindaceae with 104 Species with higher densities were Guettarda combsii Urb(522) Dendropanax arboreus (L) Decne amp Planch (237) Coccoloba spicata Lundell (158)Cecropia peltata L (134) and Trema micrantha (L) Blume (108) and together formed 54of the inventoried species

NMDS (Fig 2) showed clear differences between sampling units The stress obtainedin the test (018) is probably influenced by the variability in the composition of speciesof SU4 The dissimilarity of species is a good measure to identify the distribution of theecological niche between the species The dissimilarity analysis (ANOSIM) determinedsignificant differences in the dissimilarity between the different plots indicating that betadiversity varied between sampling units In this case the variation percentage ranged from


Figure 2 Non-metric multidimensional scaling (NMDS) plot of tree species of the four sampling unitsFull-size DOI 107717peerj6974fig-2

Table 2 Results of ANOSIM comparisons of community composition among SU showing test statis-tics for global and pair-wise comparisons

r p

All SU 00714 001SU1 SU2 068 002SU1 SU3 0917 002SU1 SU4 0845 002SU2 SU3 0635 005SU2 SU4 0607 002SU3 SU4 0652 003

60 to 91 between the plots Our results showed that the plots SU1 and SU3 are theplots with a higher degree of differentiation in the composition of species and SU1 andSU2 are those with a lower percentage of differentiation (Table 2)

Statistically significant differences were observed for species richness among theevaluated sampling units It was observed that species richness decreased from SU4 toSU1 Likewise abundance showed the same pattern except for SU2 which presented thelowest abundance It was also observed that the sampling effort performed is representativefor the richness and composition of the biota of the region (between 98 and 99 for SU1SU3 and SU4 and 88 for SU2 Table 3)

Relative Importance value index (IVI)The IVIwas obtained in each of the four SU and IVI data for each of the species are presented(Fig 3) In SU1 the species with the highest IVI are Coccoloba spicata Lonchocarpusrugosus Benth Croton sp1Hippocratea excelsa Kunth and Diospyros verae-crucis StandleyRegarding SU2 the species that characterize this community considering the highestIVI were Lysiloma latisiliquum (L) Benth Bursera simaruba (L) Sarg Malvaviscusarboreus Cav Trema micrantha Metopium brownei (Jacq) Urb Simarouba glauca DCand Guettarda combsii The characteristic species of SU3 based on IVI were Guettardacombsii Hampea trilobata Stand Zuelania guidonia (Sw) Britton amp Millsp Coccoloba


Table 3 Observed and estimated species richness for all woody plants gt05 cm dbh Different lettersindicate significant differences Raref rarefaction (for 70 individuals) Sobs observed dD estimated(with 70 individuals) qDLCL qDUCL the bootstrap lower and upper confidence limits for the diversityof order q at the specified level in the setting (with a default value of 095) SCLCL SCUCL = the boot-strap lower and upper confidence limits for the expected sample coverage at the specified level in the set-ting (with a default value of 095)

SM M N Sobs qDLCL qDUCL qD SCLCL SCUCL SC

SU1 8 193 11a 940ndash1262 94a 840ndash1032 099SU2 8 70 20b 164ndash2586 1878bc 1553ndash2203 088SU3 8 808 34c 2963ndash3837 1521c 1428ndash1619 099SU4 8 1091 54d 4747ndash6053 2241db 2145ndash2338 098Total 32 2162 63

Figure 3 List of tree species with 90 of the Relative Importance Value Index (IVI) in each plot (A)SU1 (B) SU2 (C) SU3 (D) SU4


spicata Lonchocarpus rugosus Benth Lysiloma latisiliquum Bursera simaruba SwieteniamacrophyllaKingTrema micrantha andCroton sp2 Finally the species with greater relativeimportance in SU4 wereCecropia peltataDendropanax arboreus Trema micrantha Burserasimaruba Eupatorium albicaule Sch Bip ex Klatt Piscidia piscipula (L) Sarg Hameliapatens Jacq Allophylus cominia (L) Sw Lonchocarpus guatemalensis Benth Nectandrasalicifolia Kunth Coccoloba spicata Lundell Aegiphila monstrosa Moldenke Bourreriaoxyphylla Stand Verbesina gigantea Jacq and Guettarda combsii


Table 4 Soil nutrients of SU1 SU2 SU3 and SU4 Nitrogen (N) Phosphorus (P mgkg) Potassium (mgkg) Sodium (Namgkg) Calcium(Ca) soil organic matter (SOM) C org and pHplusmn standard error

SU N SOM P K Na Ca Corg pH

SU1 032plusmn (004) 466plusmn (06) 007plusmn (002) 292plusmn (05) 018plusmn (002) 293plusmn (06) 568plusmn (027) 757plusmn (006)SU2 025plusmn (004) 32plusmn (05) 005plusmn (001) 195plusmn (069) 013plusmn (001) 382plusmn (049) 523plusmn (028 773plusmn (003)SU3 019plusmn (005) 261plusmn (061) 003plusmn (001) 29plusmn (053) 012plusmn (003) 34plusmn (09) 585plusmn (055) 771plusmn (009)SU4 024plusmn (009) 327plusmn (119) 005plusmn (002) 351plusmn (122) 01plusmn (003) 17plusmn (018) 494plusmn (049) 760plusmn (003)

Table 5 Variation partitioning of woody species richness and abundance through General LinealModel (GLM) and influence of each variable in the model

Variable Total explain model Estimate Sta Error z value p

(Intercept) 177947 195533 091 0362789SU 073231 002402 3049 00001P minus049618 100638 minus0493 0621985K 001219 002337 0521 0602098Na minus090082 071579 minus1258 0208212Ca 012279 0026 4723 232Endash06Corg minus007272 002142 minus3395 0000686

Richness 721

pH 005628 024927 0226 0821389(Intercept) 654206 507398 1289 019728SU 047363 005821 8136 408E-16P 674966 276212 2444 001454K 005896 005884 1002 031634Na minus472098 204024 minus2314 002067Ca 018468 00689 2681 000735Corg minus014126 005598 minus2524 001162

Abundance 602

pH minus069346 065187 minus1064 028742

Diversity and abundanceThe species richness and conditions of the sampling units considering the disturbancefrequency resulted in significant differences SU3 showed almost twice the number ofspecies found in SU1 and SU2 As expected SU4 was the site with the highest speciesrichness (Table 3) Table 4 summarizes soil characteristics Soil organic matter and Nwere excluded from the analysis as those values indicated collinearity gt10 GLM showed astrong correlation between the species richness of tree species Variables which explainedbest species richness were site conditions followed by Ca and soil organic matter AlsoGLM showed that abundance resulted in a strong correlation with site conditions and soilcharacteristics Species abundance was best explained by site conditions P Ca and organicC (Table 5)

DISCUSSIONThe floristic composition in the all evaluated sampling units (SU1 to SU4) was representedmainly by species of the Fabaceae This agrees with results of secondary vegetation studies


carried out in the Yucataacuten Peninsula (Mizrahi Ramos-Prado amp Jimeacutenez-Osornio 1997Pool-Estrella 1998 Goacutengora-Chiacuten 1999 Gonzaacutelez-Iturbe Olmsted amp Tun-Dzul 2002Ceccon Saacutenchez amp Campo 2004 Islebe et al 2015) Other authors like Saacutenchez-Saacutenchezamp Islebe (2002) and Duno et al (2012) found that Fabaceae are particularly diverse inthe southern region of the Yucataacuten Peninsula due to the precipitation gradient and itsbiogeographical affinity to the biota of Central America Furthermore it has been widelyreported that it is the dominant family in secondary vegetation at different successionalstages (Saacutenchez amp Islebe 1999 Flores amp Bautista 2012 Loacutepez-Martiacutenez et al 2013 Valdez-Hernaacutendez et al 2015)

The species with the highest densities recorded in the sampling units is a groupof species with resprouting capacities C spicata L rugosus Croton sp1 H trilobata Bsimaruba G combsii Croton sp2 (SU1 and SU2) characteristic of degraded areas SitesSU3 (fern with cutting removal) and SU4 (bracken free) presented the highest IVI valuesof species with seed reproduction (L latisiliquum M brownei P ellipticum C peltata Nsalicifolia) Other studies in the Yucataacuten Peninsula found similar distribution patternsof those tree species in secondary vegetation of seasonal dry forests (Dupuy et al 2012Valdez-Hernaacutendez et al 2014 Valdez-Hernaacutendez et al 2019) Differential successionalroutes can be observed depending on the origin of the disturbance (Ferguson et al 2003)which explains the dissimilarity in species composition between SU1-3 and SU4 The lowvalues of the IVI in most of the recorded species indicate specific traits like fast growth anddifferential adaptation to soil and site characteristics Similar conditions were observed in aseasonal dry tropical forest of northern Quintana Roo where in hurricane-damaged areasfew species dominated (Saacutenchez amp Islebe 1999)

The variation of species richness and abundance recorded by the rarefaction results isattributed to the invasion of P aquilinum and the history of land use in the area Thisreflects dominance patterns of species and therefore beta diversity (Loacutepez-Martiacutenez et al2013) The results suggest that while controlling the frequency of fires does not eradicatethe invasive species it can increase the diversity of species eg SU2 showed higherrichness than SU1 Also the low species richness can be explained by the different edaphicconditions present in each sampling unit (depth stoniness among others) Fires occasionalor frequent favor the spread of bracken fern The establishment of species in SU1 andSU2 is limited by shallow soils with little organic matter and characterized by species ofsecondary forest patches (Suazo-Ortuntildeo et al 2014 Valdez-Hernaacutendez et al 2014)

Three of the sampling units with Pteridium indicate that the recent history of landuse contributes to an understanding of the variation of species richness It has beenobserved that fires caused in areas dominated by P aquilinum tend to be more intensethan those that occur in other types of cover (Cawson et al 2018) The high frequencyof fires has a negative consequence and greater impact on tree species than on invasivespecies such as Pteridium (Roos et al 2010) The highest dissimilarity was found betweenSU1 and SU3 as a consequence of the cutting technique of P aquilinum This favoredenvironmental heterogeneity and the establishment of short-lived species as well as speciesof late successional ages


Heterogenous environmental conditions of the area explain why the age of the vegetationcould influence the results and restricts the regeneration in SU1 Probably the absence ofseed banks and the frequency of burning will eventually interrupt the succession There wasa high floristic dissimilarity among all sampling units (Table 3) The high dissimilaritiessuggest that most species of the sampling units have a high turnover rate Loacutepez-Martiacutenezet al (2013) reported that significant differences in the dissimilarity between successionalage classes indicate that the composition of the species changes during the successionFrom other studies analyzing succession in seasonal dry tropical forests in the YucataacutenPeninsula we observe a similar trend (Valdez-Hernaacutendez et al 2014)

Our results show that there is a strong relationship between species richness andabundance with the conditions of the site and some chemical soil variables In particularour results showed a direct relationship between species richness and abundance withP and Ca The positive relationship with P and Ca suggests that concentrations of bothelements are available given the dynamics of the organic matter in SU3 and SU4 which hasnot been interrupted by fire disturbances Similar soil conditions are reported by Bautistaet al (2005) The relationship between Na and Corg suggest that metabolic activity of soilmicroorganisms (Ceccon Huante amp Campo 2003 Eaton amp Lawrence 2006 Lange et al2015 Rodrigues et al 2016) are favoring the regeneration of SU3 and SU4 On the otherhand studies carried out in degraded sites found that the concentrations of Corg and Nacan be reduced for several years before the restoration of soil dynamics begins (Schlesingeramp Bernhardt 2013) which explains low species diversity and abundance in SU1 and SU2

CONCLUSIONSSampling sites with higher fire frequency had lower diversity values and observed speciesnumbers In sites without fires and bracken removal no increase in species recruitment wasobserved We observed that the control of fern cover with constant cuttings favors richnessand species composition and steps up secondary succession Specific soil conditions relatedto P and Ca were also detected as beneficiary to the successional processes

ACKNOWLEDGEMENTSWe appreciate comments by three anonymous reviewers and the collaboration of LuisCandelario Saacutenchez in field data collection and Beatrice Wallace Pearson for her invaluablesupport for the English edition

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by the National Forest Commission of Mexico (201623P0050number proyect) The funders had no role in study design data collection and analysisdecision to publish or preparation of the manuscript


Grant DisclosuresThe following grant information was disclosed by the authorsNational Forest Commission of Mexico 201623P0050

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Alberto Jean Baptiste conceived and designed the experiments performed theexperiments analyzed the data prepared figures andor tables authored or revieweddrafts of the paper approved the final draftbull Pedro A Macario conceived and designed the experiments performed the experimentsauthored or reviewed drafts of the paper approved the final draftbull Gerald A Islebe analyzed the data contributed reagentsmaterialsanalysis toolsauthored or reviewed drafts of the paper approved the final draftbull Benedicto Vargas-Larreta contributed reagentsmaterialsanalysis tools authored orreviewed drafts of the paper approved the final draftbull Luciano Pool contributed reagentsmaterialsanalysis tools approved the final draftbull Mirna Valdez-Hernaacutendez analyzed the data contributed reagentsmaterialsanalysistools prepared figures andor tables authored or reviewed drafts of the paper approvedthe final draftbull Jorge O Loacutepez-Martiacutenez conceived and designed the experiments analyzed the dataprepared figures andor tables authored or reviewed drafts of the paper approved thefinal draft

Data AvailabilityThe following information was supplied regarding data availability

Loacutepez-Martiacutenez JO (2019) Raw data of diversity abundance and soil samples (VersionFinal version) [Data set] PeerJ Zenodo httpdoiorg105281zenodo2649736

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj6974supplemental-information

REFERENCESBautista F Palacio G Ortiz M Batllori E Castillo M 2005 El origen y el manejo

maya de las geoformas suelos y aguas en la Peniacutensula de Yucataacuten In Bautista-Zuacutentildeiga F Palacio eds Caracterizacioacuten y manejo de los suelos de la Peniacutensula deYucataacuten implicaciones agropecuarias forestales y ambientales Meacuterida Univ Aut deCampeche Univ Aut de Yucataacuten Inst Nal de Ecologiacutea Meacutexico 21ndash32

Cawson JG Duff TJ SwanMH Penman TD 2018Wildfire in wet sclerophyll foreststhe interplay between disturbances and fuel dynamics Ecosphere 9(5)e02211DOI 101002ecs22211


Ceccon E Huante P Campo J 2003 Effects of nitrogen and phosphorus fertilization onthe survival and recruitment of seedlings of dominant tree species in two abandonedtropical dry forests in Yucataacuten Mexico Forest Ecology and Management 182(1ndash3)387ndash402 DOI 101016S0378-1127(03)00085-9

Ceccon E Saacutenchez S Campo J 2004 Tree seedling dynamics in two abandoned tropicaldry forests of differing successional status in Yucataacuten Mexico a field experimentwith N and P fertilization Plant Ecology 170(2)277ndash285DOI 101023BVEGE00000216996315147

Chambers J 2008 Software for data analysis programming with R New York SpringerClarke KR Gorley RN 2006 Primer V6 user manualmdashtutorial PRIMER-E Plymouth

Marine Laboratory UKCraneMF 1990 Pteridium aquilinum Available at httpwwwfsfedusdatabase feis

plants fernpteaquallhtml (accessed on 4 October 2018)Da Silva Matos SR da de S 2006 The invasion of Pteridium aquilinum and the impover-

ishment of the seed bank in fire prone areas of Brazilian Atlantic Forest Biodiversityamp Conservation 15(9)3035ndash3043 DOI 101007s10531-005-4877-z

Duno R Can-Itza LL Rivera-Ruiz A Calvo-Irabieacuten LM 2012 Regionalizacioacuten yrelaciones biogeograacuteficas de la Peniacutensula de Yucataacuten con base en los patronesde distribucioacuten de la familia Leguminosae Revista Mexicana de Biodiversidad83(4)1053ndash1072

Dupuy JM Hernaacutendez-Stefanoni JL Hernaacutendez-Juaacuterez RA Tetetla-Rangel ELoacutepez-Martiacutenez JO Leyequieacuten-Abarca E Tun-Dzul FJ May-Pat F 2012Patterns and correlates of tropical dry forest structure and composition in ahighly replicated chronosequence in Yucataacuten Mexico Biotropica 44(2)151ndash162DOI 101111j1744-7429201100783x

Eaton JM Lawrence D 2006Woody debris stocks and fluxes during succession in a drytropical forest Forest Ecology and Management 232(1ndash3)46ndash55DOI 101016jforeco200605038

Ewel JJ Putz FE 2004 A place for alien species in ecosystem restoration Frontiers inEcology and the Environment 2(7)354ndash360DOI 1018901540-9295(2004)002[0354APFASI]20CO2

Feng Y Fouqueray TD Van KleunenM 2019 Linking Darwinrsquos naturalizationhypothesis and Eltonrsquos diversity-invasibility hypothesis in experimental grasslandcommunities Journal of Ecology 107(2)794ndash805 DOI 1011111365-274513061

Ferguson BG Vandermeer J Morales H Griffith DM 2003 Post-agricultural succes-sion in El Peten Guatemala Conservation Biology 17(3)818ndash828DOI 101046j1523-1739200301265x

FletcherW Kirkwood R 1979 The bracken (Pteridium aquilinum (L) Kuhn) itsbiology and control In Dyer AF ed The experimental biology of ferns LondonAcademic Press

Flores JS Bautista F 2012 El conocimiento de los mayas yucatecos en el manejo delbosque tropical estacional las plantas forrajeras Revista Mexicana de Biodiversidad83(2)503ndash518


Frankland B 1976 Phytochrome control of seed germination in relation to the lightenvironment In Smith H ed Light and plant development London Butterworth-Heinemann 477ndash491 DOI 101016B978-0-408-70719-050035-8

Gallegos SC Hensen I Saavedra F SchleuningM 2015 Bracken fern facilitatestree seedling recruitment in tropical fire-degraded habitats Forest Ecology andManagement 337135ndash143 DOI 101016jforeco201411003

Garciacutea E 1997 Carta de climas Escala 1 1000000 seguacuten el Sistema de Koumlppen Modifi-cado por Garciacutea Available at httpwwwconabiogobmx informacion gis (accessedon October 2018)

Gibbons SM Lekberg Y Mummey DL Sangwan N Ramsey PW Gilbert JA 2017Invasive plants rapidly reshape soil properties in a grassland ecosystemmSystems2e00178-16 DOI 101128mSystems00178-16

Gliessman SR 1976 Allelopathy in a broad spectrum of environments as illus-trated by bracken Botanical Journal of the Linnean Society 73(1ndash3)95ndash104DOI 101111j1095-83391976tb02015x

Goacutengora-Chiacuten RE 1999 Levantamiento floriacutestico determinacioacuten del iacutendice de densidady el coeficiente de similitud de especies de la zona costera de Seybaplaya municipiode Champotoacuten a Hampolol municipio de Campeche Meacutexico Bachelor ThesisUniversidad Autoacutenoma de Campeche

Gonzaacutelez-Iturbe JA Olmsted I Tun-Dzul F 2002 Tropical dry forest recovery afterlong term Henequen (sisal Agave fourcroydes Lem) plantation in northern YucatanMexico Forest Ecology and Management 167(1ndash3)67ndash82DOI 101016S0378-1127(01)00689-2

Hartig K Beck E 2003 The bracken fern (Pteridium arachnoideum (Kaulf) Maxon)dilemma in the Andes of Southern Ecuador Ecotropica 93ndash13

Hsieh TC Ma KH Chao A 2016 iNEXT an R package for rarefaction and extrap-olation of species diversity (Hill numbers)Methods in Ecology and Evolution7(12)1451ndash1456 DOI 1011112041-210X12613

Islebe GA Saacutenchez-Saacutenchez O Valdeacutez-HernaacutendezMWeissenberger H 2015Distribution of vegetation types In Islebe GA Calmeacute S Leoacuten-Cortes JL Schmook Beds Biodiversity and conservation of the Yucatan Peninsula Cham Springer 39ndash53

IUSSWorking GroupWRB 2015 World reference base for soil resources 2014 update2015 International soil classification system for naming soils and creating legends forsoil maps World Soil Resources Reports No 106 FAO Rome

Kent M 2011 Vegetation description and data analysis a practical approach HobokenJohn Wiley amp Sons

LangeM Eisenhauer N Sierra CA Bessler H Engels C Griffiths RI Mellado-VaacutezquezPG Malik AA Roy J Scheu S Steinbeiss S Thomson BC Trumbore SE GleixnerG 2015 Plant diversity increases soil microbial activity and soil carbon storageNature Communications 6Article 6707 DOI 101038ncomms7707

Loacutepez-Martiacutenez JO Hernaacutendez-Stefanoni JL Dupuy JM Meave JA 2013 Par-titioning the variation of woody plant β-diversity in a landscape of secondary


tropical dry forests across spatial scales Journal of Vegetation Science 24(1)33ndash45DOI 101111j1654-1103201201446x

Macario PA 2010Meacutetodo para la restauracioacuten de aacutereas invadidas por el helechoPteridium aquilinum (L)Kuhn en el sur de Quintana Roo Available at httpwwwbiosakbecomdesarrollo_rural_sustentabledocs espanolp9pdf (accessed on30 October 2018)

MacDougall AS Turkington R 2005 Are invasive species the drivers or passengers ofchange in degraded ecosystems Ecology 86(1)42ndash55 DOI 10189004-0669

Marschner IC 2011 glm2 Fitting generalized linear models R package version 1Available at httpCRANR-projectorgpackage=glm2

Miranda F Hernaacutendez XE 1963 Los tipos de vegetacioacuten de Meacutexico y su clasificacioacutenBoletin de la Sociedad Botaacutenica de Meacutexico 2829ndash179 DOI 1017129botsci1084

Mizrahi A Ramos-Prado J Jimeacutenez-Osornio J 1997 Composition structure and man-agement potential of secondary dry tropical vegetation in two abandoned henequenplantations of Yucatan Mexico Forest Ecology and Management 96(3)273ndash282DOI 101016S0378-1127(97)00008-X

National Institute of Statistics and Geography (INEGI) 1993 Anuario estadiacutesticoQuintana Roo 1993 Aguascalientes INEGI

Olson BEWallander RT 2002 Effects of invasive forb litter on seed germina-tion seedling growth and survival Basic and Applied Ecology 3(4)309ndash317DOI 1010781439-1791-00127

Pennington TD Sarukhaacuten J 2005 Aacuterboles tropicales de Meacutexico Manual para la iden-tificacioacuten de las principales especies Meacutexico Universidad Nacional Autoacutenoma deMeacutexico Fondo de Cultura Econoacutemica

Pool-Estrella MR 1998 Estructura y fisonomiacutea de la vegetacioacuten de la zona costerade Seybaplaya municipio de Champotoacuten a Hampolol municipio de CampecheBachelor Thesis Universidad Autoacutenoma de Campeche

RDevelopment Core Team 2012 R a language and environment for statistical com-puting Vienna R Foundation for Statistical Computing Available at httpwwwR-projectorg

Rodrigues PMS Schaefer CEGR De Oliveira Silva J Ferreira JuacuteniorWG Dos San-tos RM Neri AV 2016 The influence of soil on vegetation structure and plantdiversity in different tropical savannic and forest habitats Journal of Plant Ecology11(2)226ndash236

Roos K Rollenbeck R Peters T Bendix J Beck E 2010 Growth of tropical bracken(pteridium arachnoideum) response to weather variations and burning InvasivePlant Science and Management 3(4)402ndash411 DOI 101614IPSM-D-09-000311

Rymer L 1976 The history and ethnobotany of bracken Botanical journal of the LinneanSociety 73(1ndash3)151ndash176 DOI 101111j1095-83391976tb02020x

Saacutenchez O Islebe G 1999Hurricane Gilbert and structure changes in a tropicalforest in south-eastern Mexico Global Ecology and Biogeography 8(1)29ndash38DOI 101046j1365-2699199900317x


Saacutenchez-Saacutenchez O Islebe GA 2002 Tropical forest communities in southeasternMexico Plant Ecology 158(2)183ndash200 DOI 101023A1015509832734

SchlesingerWH Bernhardt ES 2013 Biogeochemistry an analysis of global change UKAcademic Press

Schneider LC 2004 Bracken fern invasion in Southern Yucataacuten a case for land-changescience Geographical Review 94(2)229ndash241 DOI 101111j1931-08462004tb00169x

Schneider LC 2006 Invasive species and land-use the effect of land managementpractices on bracken fern invasion in the region of Calakmul Mexico Journal ofLatin American Geography 5(2)91ndash107

Schneider LC Fernando DN 2010 An untidy cover invasion of Bracken Fern in theshifting cultivation systems of southern Yucatan Mexico Biotropica 42(1)41ndash48DOI 101111j1744-7429200900569x

SousaM Cabrera EF 1983 Listados floriacutesticos de Meacutexico In II Flora de Quintana RooInstituto de Biologia Mexico City UNAM Meacutexico

Standley PC Steyermark JA 1958 Flora of Guatemala Chicago Chicago Museum ofNatural History DOI 105962bhltitle2270

Suazo-Ortuntildeo I Lopez-Toledo L Alvarado-Diacuteaz J Martinez-RamosM 2014 Land-use change dynamics soil type and species forming mono-dominant patches thecase of Pteridium aquilinum in a neotropical rain forest region Biotropica 47(1)1ndash9DOI 101111btp12181

Taylor JA 1989 Bracken toxicity and carcinogenicity as related to animal and humanhealth papers given at a meeting held at the UCNW Bangor Wales UK on 28th 1988Wales International Bracken Group

Tolhurst KG Turvey ND 1992 Effects of bracken (Pteridium esculentum (forst f)cockayne) on eucalypt regeneration in west-central Victoria Forest Ecology andManagement 54(1ndash4)45ndash67 DOI 1010160378-1127(92)90004-S

Valdez-HernaacutendezM Gil-Medina R Loacutepez-Martiacutenez JO Torrescano-Valle NCabanillas-Teraacuten N Islebe GA 2019 Succession and the relationship betweenvegetation and soil in the marl quarries of the Yucataacuten peninsula Mexico Forests10(2)Article 116 DOI 103390f10020116

Valdez-HernaacutendezM Gonzalez-Salvatierra C Reyes C Jackson P Andrade JL 2015Physiological ecology of vascular plants In Islebe GA Calmeacute S Leoacuten-Corteacutes JLSchmook B eds Biodiversity and conservation of the Yucatan Peninsula New YorkSpringer

Valdez-HernaacutendezM Saacutenchez O Islebe GA Snook LK Negreros-Castillo P 2014Recovery and early succession after experimental disturbance in a seasonallydry tropical forest in Mexico Forest Ecology and Management 334331ndash343DOI 101016jforeco201409018

Vandermeer JH 1972 Niche Theory Annual Review of Ecology and Systematics3107ndash132 DOI 101146annureves03110172000543

Wright AC 1967 El reconocimiento de los suelos de la Peniacutensula de YucataacutenChapingo Colegio de Postgraduados


Wyatt-Smith J Foenander EC 1962 Damage to regeneration as a result of loggingMalayan Forester 2540ndash44

Zuur AF Hilbe JM Ieno EN 2013 A beginnerrsquos guide to GLM and GLMM with R afrequentist and bayesian perspective for ecologists Newburgh Highland StatisticsLimited


environmental and soil conditions have helped to colonize almost all terrestrial ecosystemsexcept for deserts (Gliessman 1976 Taylor 1989) They have an underground rhizomewhich branches into long and short buds can grow up to 2 m in a single season whichgives it a great capacity for colonization (Fletcher amp Kirkwood 1979) Additionally throughthe creation of a physical barrier generated by the density of its canopy it hinders theestablishment of native species (Olson amp Wallander 2002) Similarly it has been observedthat the accumulation of biomass from the dry fronds modifies the frequency and intensityof fires due to the increase of available fuel (Frankland 1976 Crane 1990) This exhauststhe seed bank and limits the growth of seedlings (Da Silva Matos SR da de 2006) Thelack of competitors for limiting resources (Vandermeer 1972) the absence of pests andherbivory and their resistance to fire due to their ability to regrow from their rhizomesgive them strategic advantages over native species (Tolhurst amp Turvey 1992) Studies fromBrazil Ecuador the Dominican Republic and Rwanda found that former active agriculturalregions are currently held back due to the interruption of secondary succession processes(Hartig amp Beck 2003Gallegos et al 2015) InMexico most of the studies have been carriedout in the south mainly in the states of Quintana Roo Campeche and Oaxaca (Schneider2006 Suazo-Ortuntildeo et al 2014) Likewise it has been observed that the lack of strategiesfor their control can generate a substantial growth in a relatively short time eg Schneideramp Fernando (2010) found in the Calakmul reserve that their coverage increased from 40km2 to 80 km2 between 1982 and 2010 It was also observed that landscapes with invadedareas are less productive have a reduced biological diversity and show severe impacts inthe socio-economic dynamics of the affected regions because the areas cannot be usedby the owners (Schneider 2004 Schneider 2006 Suazo-Ortuntildeo et al 2014) Currentlyinsufficient studies have been developed in seasonally dry tropical forests that provideinformation on the historical effect and management of areas invaded by P aquilinumand its impact on the richness and floristic composition and their influence on successionStrategies are needed to restore areas affected by one of the most important invasive speciesin the world It is important to mention that the establishment of invasive species affectsthe possibility of maintaining the net primary production of the ecosystems (Ewel amp Putz2004 Gibbons et al 2017 Feng Fouqueray amp Van Kleunen 2019) Consequently the aimof this work was to determine the effect of the invasion of P aquilinum on secondarysuccession in a seasonally dry tropical forest

MATERIALS amp METHODSStudy siteThe study was carried out in the ejido (communally managed land) Laguna Om (minus8915W1870Nminus8887W 1840NWGS 84) in the south of the state of Quintana Roo Mexico withan area of 84998 ha (Fig 1) The ejido is located in the geological formation called Peteacutenwhich belongs to the Paleocene-Eocene and is characterized by massive compact macroand microcrystalline limestones which have yellow to white coloring with brown partsstained by iron oxides (Wright 1967 INEGI 1993) The terrain is flat with an undulatedmicrorelief and with wide depressions that present small plains Its altitude above sea levelvaries between 100 and 150 m (Garciacutea 1997 INEGI 1993 IUSS Working Group WRB















Treesabundances

Totalabundances










r p



















Richness 721


Abundance 602

pH minus069346 065187 minus1064 028742








































































































Treesabundances

Totalabundances










r p



















Richness 721


Abundance 602

pH minus069346 065187 minus1064 028742





























































































r p



















Richness 721


Abundance 602

pH minus069346 065187 minus1064 028742








































































































Richness 721


Abundance 602

pH minus069346 065187 minus1064 028742



























































































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