• No se han encontrado resultados

Tuxtlas Biosphere Reserve, Veracruz, Mexico

N/A
N/A
Protected

Academic year: 2019

Share "Tuxtlas Biosphere Reserve, Veracruz, Mexico"

Copied!
10
0
0

Texto completo

(1)

Availableonlineatwww.sciencedirect.com

Revista

Mexicana

de

Biodiversidad

www.ib.unam.mx/revista/ RevistaMexicanadeBiodiversidad88(2017)136–145

Ecology

Soil

nematodes

associated

with

different

land

uses

in

the

Los

Tuxtlas

Biosphere

Reserve,

Veracruz,

Mexico

Nematodos

del

suelo

asociados

a

diferentes

usos

del

suelo

en

la

Reserva

de

la

Biosfera

Los

Tuxtlas,

Veracruz,

México

Francisco

Franco-Navarro

a,

,

Damaris

Godinez-Vidal

b

aProgramadeFitopatología,ColegiodePostgraduados-CampusMontecillo,Km.36.5CarreteraMéxico-Texcoco,56230Montecillo,Texcoco,EstadodeMéxico,

Mexico

bDepartamentodeBiologíaMoleculardePlantas,InstitutodeBiotecnología,UniversidadNacionalAutónomadeMéxico,Av.UniversidadNúm.2001,Col.

Chamilpa,62210Cuernavaca,Morelos,Mexico

Received21January2016;accepted29August2016 Availableonline21February2017

Abstract

Modificationofabove-groundlanduseleadstomanychangesinthebelow-groundrhizosphere.Astudywasconductedofsoilnematodesand theirdiversityassociatedwithdifferentlandusesintheBiosphereReserveLosTuxtlas,Mexico.Threesiteswereselectedtoinvestigate4typesof landuses:naturalforest,secondaryforest,pasture,andmaizefields.Totalabundanceofnematodesandestimatorsbasedongenericanddiversity indiceswereassessedandcomparedbetweenthe4landusesandsites.Fifty-threefamiliesand124generaofnematodeswereidentifiedfromthe studyarea.ThedominantfamilieswereCriconematidae,Hoplolaimidae,Cephalobidae,andTylenchidae,andthemostabundantgenerainthis studywereHelicotylenchus,Discocriconemella,Tylenchus,SteinernemaandMesocriconema.Thegreatestnematodeabundance,genericrichness, anddiversitywerefoundinnaturalforest,closelyfollowedbysecondaryforest.Intensive(largelymonocrop)agriculturalsystems,representedby maizefieldsandpasture,hadlowgenericrichnessandsignificantlylessdiversitythannon-disturbedsystems.Mostoftheestimatorsandindices wereusefulinshowingthesignificanteffectsofdifferentlandusesonsoilnematodesinLosTuxtlas,Mexico.Thisstudyisthefirstofitstype tobecarriedoutintheBiosphereReserveLosTuxtlas,beingthefirstreportofsoilnematodesthatshowstheeffectsofthelandusechangesthat havebeenmadeinrecentyears.

©2017UniversidadNacionalAutónomadeMéxico,InstitutodeBiología.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Keywords: Below-groundbiodiversity;Neotropicalrainforest;Nematodesecology;Soildisturbance

Resumen

Lasmodificacionesenelusodesueloyenlavegetaciónconducenavarioscambiosenlarizosferadelasplantas.Sellevóacabounestudiocon elfindeconocerlosnematodosdelsueloysudiversidad,asociadosadiferentesusosdesueloenlaReservadelaBiosferaLosTuxtlas,México. Seseleccionaron3sitioscon4tiposdeusodesuelo(bosquenatural,bosquesecundario,pastizalymaizal).Paralos4usosdesuelosecalcularon ycompararontantolaabundanciatotaldenematodoscomoalgunosestimadoresbasadosengéneroseíndicesdediversidad.Seidentificaron53 familiasy124génerosdenematodosdentrodeláreadeestudio;lasfamiliasdominantesfueronCriconematidae,Hoplolaimidae,Cephalobidae y Tylenchidae y losgéneros más abundantes en elpresente estudio fueron Helicotylenchus, Discocriconemella, Tylenchus, Steinernema y

Mesocriconema.Lamayorabundanciadenematodos,riquezadegénerosydiversidad,sepresentaronenelbosquenatural,seguidoporelbosque secundario.Enlossistemasagrícolasintensivos,representadosporlospastizalesylosmaizales,lariquezadegénerosyladiversidadfueron menores,elloencomparaciónconloobservadoenlossistemasmenosperturbados.Lamayoríadelosestimadoreseíndicesdediversidadfueron

Correspondingauthor.

E-mailaddress:ffranco@colpos.mx(F.Franco-Navarro).

PeerReviewundertheresponsibilityofUniversidadNacionalAutónomadeMéxico.

http://dx.doi.org/10.1016/j.rmb.2017.01.002

(2)

útilesparaestablecer,demanerasignificativa,losefectosdediferentesusosdesuelosobrelosnematodosedáficosenLosTuxtlas,México.El presenteestudioeselprimeroensutipoqueserealizaenlaReservadelaBiosferaLosTuxtlas,yaquerepresentaelprimerreportesobrela nematofaunaedáficaendichazona,reflejandolosefectosqueconllevaelcambiodeusodesueloquehavenidosucediendoenlosúltimosa˜nos. ©2017UniversidadNacionalAutónomadeMéxico,InstitutodeBiología.EsteesunartículoOpenAccessbajolalicenciaCCBY-NC-ND (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Palabrasclave: Biodiversidaddebajodelsuelo;Bosquelluviosoneotropical;Ecologíadenematodos;Alteracióndelsuelo

Introduction

Nematodes are ubiquitous inhabitants of soilsystems due

totheir abundance, large numberof species, adaptive

strate-gies,functionalityinmulti-trophicgroups,andtheircontribution

tosoil biomass (Ettema &Bongers, 1993; Laakso &Setälä,

1999;Neher&Campbell,1996;Pen-Mouratov,Rakhimbaev, &Steinberger,2003;Yeates,Ferris,Moens,&vanderPutten,

2009).Nematodesareimportantcomponentsofthedetritusfood

webs(Freckman,1988;Sohlenius,Bostrom,&Sandor,1987),

andhabitatdisturbancesaffectingthesoilmicroenvironmentand

foodresourcescancausechangesintheirdiversity(Freckman&

Ettema,1993).Variousstudieshavedemonstratedthatnematode

abundanceoften declinessignificantly when primary

ecosys-temsaredisturbed(Ferris,Bongers,&deGoede,2001;Griffiths,

Daniell,Donn,&Neilson,2012;Hodda,Bloemers,Lawton,& Lambshead,1997;Zhao&Neher,2013),whereasdisturbance

bycultivationinagroecosystemsmaycauseanincreasein

abun-dance,probablyduetoresourcesprovidedbyincorporationof

cropwastes(Freckman&Ettema,1993).

Nematodeshavebiologicalcharacteristicsandattributesthat

associate them with ecological processes in soil, including

mineralizationofplantnutrients,nutrientcycling,and

decom-position of organic matter (Griffiths,1994; Liang,Lavian, &

Steinberger, 2001; Neher, 1999, 2001; Thornton & Matlack,

2002),which allow them tobe used as biologicalindicators

of disturbances that occur in terrestrial ecosystems (Baxter,

Rowan,McKenzie,&Neilson,2013;Ettema&Bongers,1993; Freckman& Ettema, 1993; Griffiths et al., 2012; Ito, Araki, Komatsuzaki,Kanedo,&Ohta,2015).

Fewrecentrecordsexistconcerningthenematodesassociated

withMexicanplantcommunities(Zullini,1973,1977a,1977b)

or the diversity of nematodes in Mexican Reserves(

Mundo-Ocampo,Dorado,Baldwin,Morales,&Nadler,2001),andnone

ofthesestudiesinvestigatetheimpactoflandusechangesonsoil

nematodesthatmayhaveoccurredinthoseareas.Thepresent

studyisnotonlyaninventoryofsoilnematodesfromthebuffer

zoneofLosTuxtlas,butitalsodocumentstheimpactof land

usechange on soilbiodiversityinone of the mostimportant

protectedareasinMexico,asmeasuredbythecompositionof

soilnematodecommunities.Acceptingthatnematodesplayan

importantroleinthefunctioningofsoilandarealsoquite

sen-sitivetochangesintheirmicroenvironment,thisstudyhasthe

followingobjectives:(i)toconductaninventoryofthesoil

nema-todesfromthebufferzoneoftheBiosphereReserveLosTuxtlas,

Veracruz,Mexico;(ii)tocalculategenericestimatorsand

diver-sityindicesbasedonsoilnematodes,and(iii)todeterminethe

effectoflandusechangesinthestudyareaonsoilnematodes

bythemeasurementofcommondiversityindices.

Materialsandmethods

Field work was conducted in the Biosphere Reserve Los

Tuxtlas (18◦10–18◦45N,94◦42–95◦27W)located in

Vera-cruz, Mexico. This reserve is the northernmost extension of

the Neotropical rain forest and is one of the protected areas

inwhichtheprocessesofdeforestationhavebeendocumented

forprolongedperiods(Dirzo&García,1992;Martínez-Ramos,

Ortiz-Rodríguez,Pi˜nero,Dirzo,&Sarukhán,2016).

Threesitesaround the reserve(López Mateos,Venustiano

Carranza,andSanFernando)werechosenand4typesofland

usewereselectedfromeachsite:naturalforest,secondary

for-est, pasture, and maize fields. Natural forest in the context

of thisstudy included thoseareaswithminimal or norecent

disturbance;secondaryforestincludedareaswithprevious

dis-turbanceeventsbutinarecoveryprocess;pastureincludedtracts

oflandsupportinggrassorsimilarvegetationeatenbydomestic

grazinganimals;andmaizefieldsthosesowedwithmaize,and

sometimesincorporatingsquashand/orbeans.

Eightsamplingpointswereestablishedineachdistinctland

usearea(32soilsamplingpointsineachlocality,96overall),

followinga gridpattern withadistance betweenpointsof at

least200m.Samplingpointswerepositionedwheregridlines

crossed and8 soil cores(of approximately 100g each) were

takenfromeachsamplingpointatadepthof0to20cm,usinga

5cmdiametersoilaugertubedrawnfrom2imaginaryconcentric

circlesaroundeachpoint.Fourcoresweretakenontheperimeter

oftheinnercircle(3mradius)andanother4weretakenonthat

oftheoutercircle(6mradius).The8coresfromeachsampling

pointwerecombinedintoasinglesampleinaplasticbag,placed

inacoolboxtoprotectagainstoverheating,andtransportedto

thelaboratory.

Sub-samplesof300mLofsoilweretakenfromeachsample

andthenematodesthereinwereextractedbysievingandthen

bysugarflotation(Hooper,1986b).Onceextracted,nematodes

weregentlykilledbyheatingto60◦Cfor1minandthenfixed

withcold4%formalin(Hooper,1986a).Thesuspensionoffixed

nematodesfromeachsamplewasadjustedtoavolumeof10mL

andthenematodesineachof3,1mLaliquotswerecounted.The

totalnumberofnematodespersamplewasestimatedfromthe

meanofthe3counts.Aftercounting,sampleswereprocessed

bymassdehydration inordertodrawwaterout ofthe

nema-todesandreplaceitwithglycerin(Franco-Navarro,1999);100

(3)

onpermanentslidesbythewaxringmethod(Hooper,1986a)

foridentificationunderacompoundmicroscope.Ifpossible,100

nematodesfromeachsamplingsitewereidentifiedtogenus.All

thenematodesthatwerecollectedandmountedaredepositedin

theNematode Collectionof theLaboratoryof Nematologyat

theColegiodePostgraduados,CampusMontecillo.

AccumulationcurvesforgenerawereobtainedusingSpecies

Diversity&Richnesssoftware® (1998)tocomparerichnessof

generaamonglanduses.Todeterminetheinventory

complete-nessat the generic level for each land use,3 estimates were

used:Chao2,Jacknifeandbootstrap(Colwell&Coddington,

1995).Comparisonofabundanceandgenericevennessamong

land uses was assessed through dominance-diversity graphs,

also known as abundance-range graphs (Feinsinger, 2001).

Total abundance of nematodes and averages of generic

rich-nessperlanduse,as wellas dominance(λ)that wasused to

assessdominancein allnematode genera inthe sample with

λ=p2

i,wherepi isthe proportionof ithtaxon(McSorley

&Frederick,1996;Pen-Mouratov&Steinberger,2005),were

alsoestimated.Thediversityofsoilnematodegenerawas

mea-sured with2 indices using the Species Diversity& Richness

software® (1998):(1) Simpson’s index (D), whichis heavily

weightedtowardthe mostabundantspecies(genus)ina

sam-ple(whereD=1/C,C=p2i,pi2=Ni(Ni−1)/NT(NT−1),

withNi asthe numberofindividuals inthe ithgenusandNT

as the totalnumber of individuals inthe sample) (Freckman

&Ettema,1993),and(2)Shannon–Wienerindex(H),anindex

weightedtowardrarespecies(genera)(whereH=−pi(lnpi),

pibeingtheproportionofeachtaxon(genus)inthetotal

popula-tion)(McSorley&Frederick,1996;Pen-Mouratovetal.,2003;

Pen-Mouratov&Steinberger,2005).

Totalabundance,genericrichness,dominance,andgeneric

diversity of soil nematodes by land use were compared

by means of analysis of variance (Anova) and

compar-isons of means were tested using Tukey’s studentized

range (HSD) test. All statistical procedures were

per-formed using Statistical Analysis System software (SAS,

2005;http://www.sas.com/es mx/software/analytics/stat.html);

differenceswithp<0.05wereconsideredsignificant.

Results

One hundred and twenty-four genera belonging to 13

orders and53 families were identified;only 6 morph genera

ofnematodescouldnotbeidentifiedtogenuslevel (Table1).

Onehundredandfourgenerawerecollectedinnaturalforest,

90insecondaryforest,107inpasture,and79inmaizefields

(Table2).From the overallgeneracollected,8 weredetected

onlyinnatural forest(Paraphanolaimus,Desmocolex,

Odon-topharynx, Epidorylaimus, Bursiella, Pellioditis, Aorolaimus, Hemicycliophora),3onlyinsecondaryforest(Labronema, Bas-tiana,Microlaimus),9 onlyin pasture (Dactyluroaxonchium, Oxybelondira,Takamangai,Ironus,Stenonchulus,Alloionema, Panagrocephalus, Panagrolaimus, Coslenchus) and 5 only

in maize fields (Anchidiplogaster, Acephadorylaimus,

Car-charolaimus,Crustorhabditis,Panagrobelus).Sixty-onegenera

occurredatsitescharacterizedbyall4land-uses(Table1).

140

120

100

80

60

40

20

0

1 21

Sampling points

Number of gener

a

41 61 81 101

Natural forest

Total Secondary forest Pasture fields Maize fields

Figure1.Accumulationcurveforgeneraofsoilnematodesassociatedwith fourlandusesinsidetheBiosphereReserveLosTuxtlas,Veracruz,Mexico.⇑ indicatessamplingpointsperlanduse(n=24).Total=allsamplestakeninthe studyarea(n=96).

Families with the greatest abundance across all land

uses were: Criconematidae>Hoplolaimidae>Cephalobidae>

Tylenchidae. The most abundant genera in this study were:

Helicotylenchus, the dominant genus in pasture and maize

fields,Discocriconemella,whichwasdominantinnaturaland

secondary forests,Tylenchus,an herbivore withhigh relative

abundances in all land uses but particularly in pasture, and

Steinernema,a bacterial feeder andentomopathogenic

nema-tode with high values in both natural and secondary forests

(Table1).Thegenerawiththelowestdensitiesoverallin

sam-pled siteswereIronus,Carcharolaimus, Crustorhabditis,and

Stenonchulus(Table1).

Atotalof97,054soilnematodeswereextractedfromallsoil

samples(n=96);33%innaturalforest,31%inpasture,21%in

secondaryforestand15%inmaizefields.Totalabundanceof

soilnematodesbylanduse(n=24)wassignificantlydifferent

(p<0.05,F=3.23)betweennaturalforest(32,018individuals)

andmaizefields (14,095individuals),butnostatistically

sig-nificantdifferenceswerefoundbetweennaturalforest,pasture

(30,295individuals),andsecondaryforest(20,646individuals)

(p>0.05, F=2.16), despite the presence of more nematodes

in the natural forest (5.3% and 35.5% more, respectively)

(Table1).Averagegenericrichnessshowedsignificant

differ-ences (p<0.001, F=6.84) amongland useswith the highest

average in natural forest (26), followed by secondary forest

and pasture (20 in both cases), and maize fields (18).

Con-versely,dominanceofgenerawassignificantlyhigher(p<0.05,

F=3.76) in pasture (0.23±0.06) than in secondary forest,

maize fields, andnatural forest (0.17±0.04, 0.17±0.03and

0.14±0.03,respectively).

Genericaccumulationcurvesforalllandusesdidnotreach

anasymptotebutalllandusesmayhavereachedaplateauwith

morethan100samples(Fig.1).Diversityestimatesindicated

that,innaturalforest,morethan89%ofthegenerapresentwere

(4)

Table1

NematodegeneraassociatedwithfourlandusesinLosTuxtlas,Veracruz,Mexico,andtheirabundancein96soilsamples(300mL)takenandanalyzedfromthe studyarea.

Family/genus Landuses

Naturalforest(n=24) Secondaryforest(n=24) Pasture(n=24) Maizefields(n=24) Achromadoridae

Achromadora 238 126 183 60

Actinolaimidae 0 0 10 12

Aetholaimidae

Aetholaimus 0 9 0 3

Alaimidae

Alaimus 287 146 95 248

Amphidelus 7 0 33 0

Paramphidelus 195 23 92 0

Alloionematidae

Alloionema 0 0 7 0

Anguinidae

Ditylenchus 43 0 35 90

Aphelenchidae

Aphelenchus 641 396 569 953

Aphelenchoididae

Aphelenchoides 459 179 130 130

Aporcelaimidae

Aporcelaimium 766 490 678 203

Paraxonchium 107 49 49 176

Takamangai 0 0 10 0

Bastianiidae

Bastiania 0 11 0 0

Dintheria 15 18 4 13

Belondiridae

Axonchium 344 143 158 54

Belondira 165 303 473 40

Belondirella 7 20 54 0

Dactyluroaxonchium 0 0 8 0

Belondiridae

Oxybelondira 0 0 18 0

Phallaxonchium 0 11 7 0

Belondiroidea 7 0 6 7

Belonolaimidae

Trophorus 164 329 70 193

Carcharolaimidae

Carcharolaimus 0 0 0 3

Cephalobidae

Acrobeles 673 501 622 519

Acrobeloides 525 580 1,176 546

Cephalobus 179 30 52 144

Cervidellus 50 19 69 63

Chiloplacus 82 125 85 0

Eucephalobus 54 127 100 41

Heterocephalobus 776 557 595 260

Panagrocephalus 0 0 18 0

Teratolobus 24 41 17 0

Chambersiellidae

Macrolaimellus 7 14 0 0

Microlaimus 0 11 0 0

Trualaimus 0 14 8 0

Criconematidae

Criconema 632 569 19 60

(5)

Table1(Continued)

Family/genus Landuses

Naturalforest(n=24) Secondaryforest(n=24) Pasture(n=24) Maizefields(n=24)

Criconemoides 267 32 3 20

Crossonema 17 7 0 0

Discocriconemella 7,081 3,839 133 412

Hemicycliophora 179 0 0 0

Mesocriconema 561 3,100 542 767

Ogma 317 142 0 0

Desmocolecidae

Desmocolex 59 0 0 0

Diphterophoridae

Diphterophora 0 3 0 4

Diplogasteridae

Anchidiplogaster 0 0 0 7

Butlerius 13 11 33 13

Diplogasteridae

Metadiplogaster 91 0 10 0

Pareudiplogaster 105 36 21 49

Diploscapteridae

Diploscapter 201 252 1,064 218

Drilonematidae

Drilocephalobus 115 40 300 0

Dorylaimidae

Amphidorylaimus 41 0 59 0

Coomansinema 64 0 22 3

Laimydorus 11 0 44 0

Mesodorylaimus 347 35 168 121

Prodorylaimus 1,262 623 765 158

Dorylaimoidea 14 0 4 0

Halaphanolaimidae

Aphanolaimus 711 157 228 127

Paraphanolaimus 9 0 0 0

Heteroderidae

Meloidogyne 523 130 276 230

Hoplolaimidae

Aorolaimus 60 0 0 0

Helicotylenchus 2,100 1,541 11,659 2,516

Rotylenchulus 222 83 20 30

Ironidae

Ironus 0 0 4 0

Monhysteridae

Eumonhystera 11 10 11 8

Monhystera 137 0 36 120

Mononchidae

Comiconchus 0 12 7 0

Iotonchus 90 3 74 93

Miconchus 123 91 24 33

Mononchus 72 45 63 39

Prionchulus 135 29 73 26

Mylonchulidae

Mylonchulus 175 94 92 50

Neodiplogasteridae

Pristionchus 143 13 29 29

Nordiidae

Acephadorylaimus 0 0 0 11

(6)

Table1(Continued)

Family/genus Landuses

Naturalforest(n=24) Secondaryforest(n=24) Pasture(n=24) Maizefields(n=24)

Oriverutus 51 14 3 7

Paroriverutus 0 0 166 60

Nygellidae

Nygellus 0 46 147 6

Nygolaimellidae

Aporcelaimoides 258 11 77 148

Nygolaimidae

Aquatides 112 0 197 5

Nygolaimus 58 11 47 0

Odontopharyngidae

Odontopharynx 14 0 0 0

Onchulidae

Stenonchulus 0 0 3 0

Panagrolaimidae

Panagrobelus 0 0 0 7

Panagrolaimus 0 0 10 0

Plectidae

Anaplectus 318 201 116 26

Plectus 165 90 375 148

Plectinae1 105 14 0 0

Plectidae

Plectinae2 49 0 25 0

Wilsonema 4 3 6 7

Pratylenchidae

Pratylenchus 121 81 307 553

Prismatolaimidae

Prismatolaimus 461 352 792 302

Pseudodiplogasteroididae 105 36 21 49

Pseudodiplogasteroides 413 146 403 134

Qudsinematidae

Allodorylaimus 119 68 50 127

Epidorylaimus 11 0 0 0

Eudorylaimus 145 0 25 0

Labronema 0 11 0 0

Microdorylaimus 215 243 108 12

Thorneella 374 62 174 37

Rhabditidae

Bursiella 21 0 0 0

Crustorhabditis 0 0 0 4

Dolichorhabditis 29 21 4 0

Mesorhabditis 419 199 481 481

Paradoxorhabditis 111 21 56 30

Pellioditis 8 0 0 0

Prodontorhabditis 628 81 142 42

Protorhabditis 143 53 108 95

Rhabditella 40 23 28 61

Rhabditidae 0 21 6 0

Rhabpanus 17 0 7 0

Stomachorhabditis 59 0 64 4

Teratorhabditis 175 16 22 31

Xylorhabditis 62 0 130 36

Rhabditonematidae

Rhabditonema 75 44 477 61

Rhabdolaimidae

(7)

Table1(Continued)

Family/genus Landuses

Naturalforest(n=24) Secondaryforest(n=24) Pasture(n=24) Maizefields(n=24) Steinernematidae

Steinernema 1,468 1,735 751 776

Teratocephalidae

Euteratocephalus 10 0 22 0

Steratocephalus 18 4 3 0

Teratocephalus 42 24 92 0

Trichodoridae

Trichodorus 25 7 0 0

Tripylidae

Tripyla 113 50 30 29

Tripylina 65 7 0 0

Trischistoma 66 26 33 56

Tylenchidae

Coslenchus 0 0 29 0

Psilenchus 0 42 176 72

Tylenchus 2,531 1,305 2,770 1,492

Tylenchulidae

Gracilacus 70 99 6 7

Paratylenchus 352 92 283 302

Xiphinematidae

Xiphinema 520 197 311 35

Total 32,018a 20,646a 30,295a 14,095b

82%,respectively,andinmaizefieldsmorethan78%.The

esti-matespredictthatasmanyas147generacouldberecordedfor

soilnematodesfromallsitesstudied(Table2).

Indominance-diversitygraphsforeachlanduse,slopeswere

similar,althoughneithertheabundancedistributionpatternnor

thehierarchicalorderofgeneraweresimilar(Fig.2).In

natu-ralforest,1 genuswashighlydominant (Discocriconemella),

4 were moderately dominant (Tylenchus, Helicotylenchus,

SteinernemaandProdorylaimus),and3weremoderately low

in abundance (Macrolaimellus, Amphidelus, and Belondira),

whereas in secondary forest 2 genera were dominant (

Dis-cocriconemellaandMesocriconema),3weremoderatelyhighin

abundance(Steinernema,Helicotylenchus,andTylenchus),and

3hadlowabundance(Stenonchulus,Iotonchus,andWilsonema)

(Fig. 2). In pasture, only 1 genus was notably abundant

(Helicotylenchus) and 3 were moderately high in abundance (Tylenchus,Acrobeloides,andDiploscapter).Finally,inmaize

fields, 3 genera were the most abundant (Helicotylenchus,

Tylenchus,andAphelenchus),2 generaweremoderately high

inabundance(SteinernemaandMesocriconema),and3genera

hadlowabundance(Coomansinema,Aetolaimus,and

Carcharo-laimus)(Fig.2).

Whensoilnematodesinthisstudywereassignedtotrophic

groups, plant parasitic nematodes andbacterial feeders were

the mostabundantanddominant,followedbyfungalfeeders,

omnivores,andfinallypredators.Overall,thegreatestnumber

ofbacterialfeederswascollectedfrompastureandmaizefields;

asimilartendencywasobservedwithfungalfeedersbut,inthis

case,thegreatestnumberwascollectedfrommaizefields

fol-lowedbypasture.Omnivoresandpredatorsshowedthegreatest

numbers innaturalandsecondaryforest,whereasthegreatest

numbers of plant parasitic nematodes were observed in

sec-ondary forest,followed by natural forest,pasture, andmaize

fields. A deeper analysis of the trophic structure of the soil

nematodecommunitieswillbemadeinsubsequentstudies.

ThehighestSimpson’sindexwasobservedinnaturalforest

(9.45±1.73),significantly greater(p<0.05,F=3.76)thanin

pasture (6.28±1.19) butnotsignificantly differentfrom

sec-ondaryforestandmaizefields(p>0.05,F=2.08)(7.58±1.34

and7.42±1.22,respectively)(Fig.3).ForShannon’sindex,the

Table2

Observedandestimatedgenericrichnessofsoilnematodesassociatedwith4landusesandalltypesoflandusesinLosTuxtlas,Veracruz,Mexico.

Generarichness Alllanduses Naturalforest Secondaryforest Pasture Maizefields

Observed 130 104 90 107 79

Chao2 130 104 90 107 79

Bootstrap 137.9 110.2 100.3 118.5 88.7

Jacknife 146.8 116.5 112 131.2 101.1

(8)

0

–0.5

–1

He He

He

P S S

S

Ac Ap

Ae

O Io

Ste Ste

Str W W

Co

Ca Be Amp

Mac He

Ty Ty

Ty Ty Dis Dis

–1.5

–2

–2.5

–3

–3.5

–4

–4.5

Dip Me Me

Natural forest Secondry forest Maize Pasture

Log 10 (ni/N)

Figure 2.Dominance-diversity graphs for soil nematodes associated with 4 land uses inside the Biosphere Reserve Los Tuxtlas, Vera-cruz, Mexico. Dis=Discocriconemella, Me=Mesocriconema, S=Steinernema, He=Helicotylenchus, Ap=Aphelenchus, Ty=Tylenchus, Ac=Acrobeloides, Dip=Diploscapter, P=Prodorylaimus, Str=Steratocephalus, Io=Iotonchus, W=Wilsonema, Mac=Macrolaimellus, Amp=Amphidelus, Be=Belondira, O=Oriverutus,Ste=Stenonchulus,Co=Coomansinema,Ae=Aetolaimus,Ca=Carcharolaimus.Ni=numberofindividualsofeachgenus;N=numberofindividuals ofallspecies.

12

10

ab a

ab b

8

6

4

2

0

Natural forest Secondary forest

Land uses

Simpson’

s inde

x

Pasture fields Maize fields

Figure3.Simpson’sindexforsoilnematodesassociatedwith4landusesinside theBiosphereReserveLosTuxtlas,Veracruz,Mexico(n=24).

resultsfollowedasimilarpatterntothatoftheSimpson’sindex,

withthehighestvalueinnaturalforest(2.52±0.18),followed

bysecondaryforest(2.30±0.16)andmaizefields(2.24±0.15),

andwith the lowestindex in pasture (2.13±0.19) (p<0.05,

F=3.40)(Fig.4).

Discussion

Agriculturalmanagementpracticesandmanyotherhuman

activitiesdisturbthe soilecosystem andaffectsoilnematode

diversity(Freckman&Ettema, 1993;Itoetal., 2015; Neher,

2001;Zhao&Neher,2013).Thedifferentlandusageareas

sam-pledrepresentthemainenvironmentalrangesoflandusesinthe

3

2.5 a

a

a a

2

1.5

1

0.5

0

Natural forest Secondary forest

Land uses

Shannon inde

x

Pasture fields Maize fields

Figure4.Shannon’sindexforsoilnematodesassociatedwith4landusesinside theBiosphereReserveLosTuxtlas,Veracruz,Mexico(n=24).

BiosphereReserveLosTuxtlasthatarelikelytobeaffectedin

theirbelow-groundsoilbiodiversity.Thetransitionfrom

above-ground plantheterogeneityinnaturalforeststoextremeplant

homogeneity inagriculture isreflected in the soilnematodes

andtheirdiversity.

Despitetheobservedandestimatednumberofgenerabeing

higherforpasturethannaturalforest,thenumberofnematodes

and the average generic richness were higher in natural

for-estthanintheotherlanduses.These2parameterswereeven

higherinnatural forestthanvaluespreviouslyreportedinthe

literature(Freckman&Ettema,1993;Liangetal.,2001;

Pen-Mouratov&Steinberger,2005;Sohleniusetal.,1987).Whenthe

(9)

comparedwiththosefromotherstudies, thenumbersof

gen-eraarehigherthanthosereportedfromdifferentgeographical

areas and environments, mostly in temperate regions (Neher

&Campbell,1996;Neher,1999;Thornton&Matlack,2002; Yeates,1984).

Thegreatestgenericrichnessobtainedfromthenatural

for-estinLos Tuxtlasis similartothat inotherstudiesinwhich

richnessislowerinrecentlydisturbedsoilthaninsoilthathas

notbeen disturbedforseveraldecades (Thornton&Matlack,

2002),implyingeradicationof speciesduringthe disturbance

event (Freckman & Ettema, 1993; Hodda et al., 1997). The

greatestdominanceofgenerawasfoundinpastures,where

Heli-cotylenchus,atypical plantfeeder, wasthe maingenus.This

is acosmopolitangenus so its highabundance, as shown by

thedominance-diversitygraph,indicatesthedominanceofthis

genusoverothersoilnematodesisaresultofthegreatuniformity

ofplantscharacteristicofpasture.Althoughthedominanceof

Helicotylenchuswasobservedinmaizefieldstoo,thedifference

withrespecttothenextmostdominant genus,Tylenchus,was

lowerthanthatobtainedinpasture.Incontrasttothedisturbed

systems,innaturalforestandoccasionallyinsecondaryforest,

thedominantgenuswasDiscocriconemella,atypicalplantroot

feederintropicalregionsoftheworld.Dominanceofthisgenus

reflectsthelackofsoildisturbance,whichhasallowedthe

per-sistenceofthisnativegenusinsteadoftheexoticgenerafound

inpastureormaizefields.Whentheanalysisofbothestimates

wascombined,it wasobservedthatinnon-disturbedsystems

thenumberofgenera(genericrichness)isgreater,butwithout

an extremelydominant genus(genericdominance) abovethe

rest;inpasture,anintermediatevalueofgenericrichnesswas

combined withthe highestgeneric dominance. Thissuggests

thatinthismonocroppingsystemthelandusechangecan

elim-inatesomegeneraformerlypresentandpromotethedominance

ofother,mainlyexoticones,thuspermanentlymodifyingsoil

nematodediversityandpopulationstructure.

NematodetrophicstructureinLosTuxtlaswasdominatedby

plantparasitesandbacterialfeeders(mostlyrepresentedbythe

OrderRhabditida),asimilarsituationtothatobservedinstudies

oftemperateregions(Neher,1999;Neher&Campbell,1996;

Pen-Mouratovetal.,2003;Pen-Mouratov&Steinberger,2005; Thornton& Matlack,2002).In pasture andmaize fields,the

mostabundanttrophicgroupswerebacterialfeedersandfungal

feeders,insimilarproportionstothosefoundinother

agricul-turalsites(Freckman&Ettema,1993;McSorley&Frederick,

1996;Pen-Mouratov&Steinberger,2005).Bacterialand

fun-galfeedersaremoreabundantindisturbedsoils,suggestingthat

disturbanceimprovessubstratequalityorresourceavailability,

presumably thereby fostering growth of bacterial andfungal

prey populations(Thornton & Matlack, 2002). On the other

hand,thehighestpercentagesofomnivoresandpredatorswere

observedinnaturalforestandsecondaryforest,althoughthey

weretheleastabundantincomparisonwithothertrophicgroups.

Fromtheirpositionhigherinthesoilfoodweb,predatorsand

omnivoresmayalsohaveadirectorindirecteffecton

decom-positionbycontrollingthebiomassofmicrobivores(Laakso&

Setälä, 1999),but theyare moresensitivetosoil disturbance

thanmicrobivorous nematodes(Bongers,1990).Accordingto

ThorntonandMatlack(2002),higherpopulationsoffungaland

bacterialfeedersaredependentontheabsenceofpredators,so

thisinterrelationshipcouldexplainthepresenceandproportion

ofcolonizergroups(bacterialandfungalfeeders)withrespect

to persistent groups (omnivores and predators) in both

non-disturbedareasandinareasunderagriculturalmanagement.The

long-livednematodes,suchasomnivoresandpredators,which

weremoreabundantinhardlydisturbedandnon-disturbed

sys-tems(naturalandsecondaryforest),areassociatedwithstable

environments. However,whenthesehabitats arethenaffected

withinputsoforganicmatterand/orpollutants,orhuman

activ-ities likeagriculture(inthe caseof pasturesandcropfields),

theincreasedbacterialactivityfavorscolonizernematodesthat

feedonbacteriaandrespondquicklytochanges,whereas

persis-tersnematodes(omnivoresandpredators)decrease(Freckman

&Ettema,1993).

ThehighestvaluesofsoilnematodediversityinLosTuxtlas,

calculated using both Simpson’s index andShannon’s index,

were foundinnatural forest. In general,the diversityindices

of natural forestinthisstudy werehigher or similartothose

observedinotherlandusesandinotherreports(Freckman&

Ettema,1993;Liang,Lavian,&Steinberger,1999;Liangetal., 2001;Pen-Mouratovetal.,2003;Yeates&King,1997),which

reflects the factthat the diversityof nematodesis favoredby

littleorhardlydisturbedsoil.

In this study,the indices andgeneric estimators that were

calculated allowed some effects of land use changes on soil

nematodes and their diversity in the Mexican tropics to be

detected.Nematodeswereshowntobesensitivetoperturbation

inthisstudy area.In littledisturbedandnon-disturbed areas,

suchasnaturalforestandsecondaryforest,richnessand

diver-sity of nematodes were significantly greater than in systems

usedforcropproductionandmonocropping,suchaspastureand

maizefields.Thesimplificationofabove-groundplant

assem-blagesthereforehasdrasticeffectsonbelow-groundnematode

communitiesinasimilarmannertothatobservedinothertaxa.

This is the first report in Mexico on the changes brought

aboutbyhumanactivityonsoilnematodepopulationsand

diver-sity, both for plant-parasitic and free-living nematodes. The

presentstudysupportspreviousresultsreportedintheliterature

andcontributes toanincrease inthe knowledgeof nematode

faunaanditsdiversityinsoilsfromtheMexicantropicsandthe

changesthattheyundergoundertheinfluenceofdifferentland

usechanges.Theseresultsmayhelpmodelandpredictfuture

changes inbiodiversityandspeciesinteractionswithlanduse

change.

Acknowledgements

Theresearchwassupportedbythe“Conservationand

Sus-tainable Management of Below-Ground Biodiversity Project

(CSM-BGBD)” inMexico, which wasfunded bythe Global

Environmental Facility (GEF), implemented by the United

Nations Environment Program (UNEP), andexecuted by the

Tropical SoilBiologyandFertilityInstituteofCIAT (TSBF).

In Mexico,theproject wascoordinatedbyDr.IsabelleBarois

(10)

manuscript review is given to Dr. Ken Evans, Rothamsted

Research,Dr.HowardFerris,NematologyDepartmentat

Uni-versityofCalifornia-Davis,andDr.CasparChater,International

ResearchFellowatMolecular Biologyof PlantsDepartment,

Institutode Biotecnología,UNAM. Theauthors are indebted

toDr.AlejandroEsquivel,NationalUniversity,Heredia,Costa

Rica,forhissupportwiththeidentificationofsoilnematodes,to

Dr.JoséAntonioGarcía-PérezandBiol.MartínSantosfortheir

supportwithfieldwork, andtoMr. ArturoMartínez-Sanchez

fortechnicalassistance.

References

Baxter,C.,Rowan,J.S.,McKenzie,B.M.,&Neilson,R.(2013).Understanding soilerosionimpactsintemperateagroecosystemsbridgingthegapbetween geomorphologyandsoilecologyusingnematodesasamodelorganism. Biogeosciences,10,7133–7145.

Bongers,T.(1990).Thematurityindex:anecologicalmeasureof environ-mentaldisturbancebasedonnematodespeciescomposition.Oecologia,83, 14–19.

Colwell,R.K.,&Coddington,J.A.(1995).Estimatingterrestrialbiodiversity throughextrapolation.InD.L.Hawksworth(Ed.),Biodiversitymeasurement andestimation(pp.101–118).NewYork:Chapman&Hall.

Dirzo, R., & García,M. (1992).Rates of deforestation in Los Tuxtlas, a NeotropicalareainsoutheastMexico.ConservationBiology,6,84–90.

Ettema,C.H.,&Bongers,T.(1993).Characterizationofnematode coloniza-tionandsuccessionindisturbedsoilusingtheMaturityIndex.Biologyand FertilitySoils,16,79–85.

Feinsinger,P. (2001).Designingfieldstudies forbiodiversity conservation. Washington,DC:TheNatureConservancyandIslandPress.

Ferris,H.,Bongers,T.,&deGoede,R.G.M.(2001).Aframeworkforsoilfood webdiagnostics:anextinctionofthenematodefaunalanalysisconcept. AppliedSoilandEcology,18,13–29.

Franco-Navarro,F.(1999).Descripciónmorfológicaehistopatologíainducida porunaespeciedelgéneroGloboderaenJaltomataprocumbensenMéxico. Masterthesis.Texcoco,EstadodeMéxico,Mexico:Colegiode Postgradu-ados.

Freckman,D.W.(1988).Bacterivorousnematodesandorganic-matter decom-position.Agriculture,EcosystemsandEnvironment,24,195–217.

Freckman,D.W.,&Ettema,C.H.(1993).Assessingnematodecommunities inagroecosystemsofvaryinghumanintervention.Agriculture,Ecosystems andEnvironment,45,239–261.

Griffiths,B.S.(1994).Approachestomeasuringthecontributionofnematodes andprotozoatonitrogenmineralizationintherhizosphere.SoilUseand Management,6,88–90.

Griffiths,B.S.,Daniell,T.J.,Donn,S.,&Neilson,R.(2012).Bioindication potentialofusingmolecularcharacterizationofthenematodecommunity: responsetosoiltillage.EuropeanJournalofSoilBiology,49,92–97.

Hodda,M.,Bloemers,G.F.,Lawton,J.H.,&Lambshead,P.J.(1997).The effectsofclearingandsubsequentlanduseonabundanceandbiomassof soilnematodesintropicalforest.Pedobiologia,41,279–294.

Hooper,D.J.(1986a).Extractionoffree-livingstagesofsoil.InJ.F.Southey (Ed.),Laboratorymethodsforworkwithplantandsoilnematodes(pp. 5–30).UnitedKingdom:MinistryofAgricultureFisheriesandFood, Ref-erenceBook402.

Hooper,D.J.(1986b).Handling,fixing,stainingandmountingnematodes.InJ. F.Southey(Ed.),Laboratorymethodsforworkwithplantandsoilnematodes (pp.59–94).MinistryofAgricultureFisheriesandFood,ReferenceBook 402.

Ito, T.,Araki, M.,Komatsuzaki,M.,Kanedo, N.,&Ohta, H.(2015).Soil nematodecommunitystructureaffectedbytillagesystemsandcovercrop managementsin organicsoybeanproduction.Applied SoilEcology,86, 137–147.

Laakso,J.,&Setälä, H.(1999). Populationandecosystemleveleffectsof predationonmicrobialfeedingnematodes.Oecologia,120,279–286.

Liang,W.,Lavian,I.,&Steinberger,Y.(1999).Dynamicsofnematode commu-nitycompositioninapotatofield.Pedobiologia,43,459–469.

Liang,W.,Lavian,I.,&Steinberger,Y.(2001).Effectofagriculturemanagement onnematodecommunitiesinaMediterraneanagroecosystem.Journalof Nematology,33,208–213.

Martínez-Ramos,M.,Ortiz-Rodríguez,I.,Pi˜nero,D.,Dirzo,R.,&Sarukhán, J.(2016).Anthropogenicdisturbancesjeopardizebiodiversityconservation withintropicalrainforestreserves.ProceedingsoftheNationalAcademyof SciencesoftheUnitedStatesofAmerica,113,5323–5328.

McSorley,R.,&Frederick,J.J.(1996).Nematodecommunitystructureinrows andbetweenrowsofasoybeanfield.FundamentalandAppliedNematology, 19,251–261.

Mundo-Ocampo,M.,Dorado,O.,Baldwin,J.G.,Morales,R.C.,&Nadler,S. (2001).DiversidaddelafaunanematológicaenlaReservadelaBiosfera SierradeHuautla,Morelos,México.InAbstractsofXXXIIIannualmeeting oftheOrganizationofNematologistsofTropicalAmerica

Neher,D.A.(1999).Nematodecommunitiesinorganicallyandconventionally managedagriculturalsoils.JournalofNematology,31,142–154.

Neher,D.A.(2001).Roleofnematodesinsoilhealthandtheiruseasindicators. JournalofNematology,33,161–168.

Neher,D.A.,&Campbell,C.L.(1996).Samplingforregionalmonitoring ofnematodecommunitiesinagriculturalsoils.JournalofNematology,28, 196–208.

Pen-Mouratov,S.,Rakhimbaev,M.,&Steinberger,Y.(2003).Seasonaland spatialvariationinnematodecommunitiesinaNegevDesertEcosystem. JournalofNematology,35,157–166.

Pen-Mouratov, S., & Steinberger, Y. (2005). Spatio-temporal dynamic heterogeneityofnematodeabundanceina desertecosystem.Journalof Nematology,37,26–36.

Sohlenius,B.,Bostrom,S.,&Sandor,A.(1987).Long-termdynamicsof nema-todecommunitiesinarablesoilunderfourcroppingsystems.Journalof AppliedEcology,24,131–144.

Thornton,C.W.,&Matlack,G.R.(2002).Long-termdisturbanceeffectsin thenematodecommunitiesofSouthMississippi Woodlands.Journalof Nematology,34,88–97.

Yeates,G.W.(1984).Variationinsoilnematodediversityunderpasturewith soilandyear.SoilBiologyandBiochemistry,16,95–102.

Yeates,G.W.,Ferris,H.,Moens,T.,&vanderPutten,W.H.(2009).Therole ofnematodesinecosystems.InM.J.Wilson,&T.Kakouli-Durate(Eds.), Nematodesasenvironmentalindicators(pp.1–45).UnitedKingdom:CABI Publishing.

Yeates,G.W.,&King,K.L.(1997).Soilnematodesasindicatorsoftheeffect ofmanagementongrasslandsintheNewEnglandTablelands(NSW): com-parisonofnativeandimprovedgrasslands.Pedobiologia,41,526–536.

Zhao,J.,&Neher,D.A.(2013).Soilnematodegenerathatpredictspecifictypes ofdisturbance.AppliedSoilEcology,64,135–141.

Zullini,A.(1973).SomesoilandfreshwaternematodesfromChiapas(Mexico). SubterraneanfaunaofMexico.PartII.Roma:AccademiaNazionaledei Lincei.

Zullini, A. (1977a). Some freshwater nematodes of southern Mexico and Guatemala. Subterraneanfaunaof Mexico.Part III.Roma:Accademia NazionaledeiLincei.

Figure

Figure 1. Accumulation curve for genera of soil nematodes associated with four land uses inside the Biosphere Reserve Los Tuxtlas, Veracruz, Mexico
Figure 4. Shannon’s index for soil nematodes associated with 4 land uses inside the Biosphere Reserve Los Tuxtlas, Veracruz, Mexico (n = 24).

Referencias

Documento similar

Five new records of Glomeromycota are reported from the Neotropical region of Mexico, seven new records of AMF for Veracruz and one new record from Mexico

To fill these gaps, this study has evaluated the soil respiration, different soil physico-chemical properties, as well as plant diversity in a forest of Castilla La Mancha

Cadmium, Lead, Copper, Zinc, and Iron Concentration Patterns in Three Marine Fish Species from Two Different Mining Sites inside the Gulf of California, Mexico..

The influence of various environmental factors (altitude, slope, vegetation density and aspect) on leaf composition (nitrogen, carbon chlorophyll content and chlorophyll

[7]. This problem has acquired great relevance in Mediterranean rural landscapes. Land uses and ecosystem services, associated with their millenarian landscapes, have been drastically

The biosphere reserve model explicitly recognizes the necessity of integrating different actors into the design and implementation of effective mechanisms of biodiversity

Once in soil, the availability of these The study was carried out in 2009 in three metals is a function of some parameters like pH, clay municipalities of the State of Hidalgo,

Considering the wide cultural and language differences between Spain and Mexico, the aim of this study was to test the psychometric properties of a new version of the SURPS