This article isprotected rights by All copyright. reserved. 10.1111/plb.12868 doi: lead todifferences version between this andtheof Pleasec Version Record. been and through typesetting, proofreading whichmay thecopyediting, process, pagination This article undergone has for and buthas accepted been not review publication fullpeer Acceptedseed longevity; germination; bank. soil seed Keywords: [email protected] Salta Naturales,(LABIBO), de Ciencias Botánicas Universidad Facultad de Nacional autor: Corresponding Running head Salta Universidadde Nacional InvestigacionesLaboratorio de Naturales, Botánicas Facultad (LABIBO), de Ciencias Article AngelaGorostiague, Pablo Gutiérrez Pablo & Ortega Lindow Lucía Andes Central form seedAn Do cacti soil banks? species from using evaluation the R. Bekker Dr. Handling Editor: Articletype : Research Paper DR. ORTEGAP. - CONICET, Av.CONICET, Bolivia 4400,Salta, Argentina. 5150, e arid arid Cactaceae;environments; nurse recruitment;plant; seed - - BAES (Orcid : ID 0000 López, Guadalupe Guadalupe López, : Soil seedSoil : ban
Tel.
Pablo Ortega +54
- 0387 ks - CONICET - 0002
i Galíndez,Silvia Valeria Sühring, Pastrana n cacti - 154126628. - 3436 - Baes. LaboratorioBaes. de Investigaciones
-
6823)
- Baes
- mail: mail: ite this articleite this as
Southern - Ignes, Ignes, This article isprotected rights by All copyright. reserved. Accepted conservation for actions because manythem are of under better and dispersal seed and not onlyestablishment. by differential sugge Seed banks. density can vary microenvironmentsand between burial. Our resultsafter cactus show evidence strong that species with time,decreased longevity burial with seed always less being density wasunder potential found nurse plants. germinationSeed microenvironments populations.and among In species, some the Article of the species,62.5% 32 evaluated variation in seed finding was species determined through experiment a burial distribution32density species. and native for longevitySeed cactus for in bare and areas) sites. at 12 selected determined presence seed We Andes.sampleswere Soil Central collected seed studyingbanks, distribution, density longevity seed seed and Southern the in them.evaluated In thiswe cactus work,species analyzed seed soil whether form ca is commonlythat assumed controversy is There cactuswhether seed speciessoil Although it overbanks. form Abstract Gymnocalycium sting that cactus sting that
stand the population dynamics the stand dynamics population ofcactus
species form short form species - nurse plant associationsplant can also be nurse cti do not form seed cti doseed not verybanks,form have studies few - term seed in two nurse (under microhabitats
banks. Ourbanks. resultswill to help
threatened by activities. human . recorded We
species, groupa focal species
We that found We
density between explained by differential byexplained differential
among populations,
than 24 months than
greatestseed do seedform and see
viableseeds for -
absence, absence, six these of Echinopsis d viabilityd
plants
This article isprotected rights by All copyright. reserved. Accepted seed term persistent banks (Thompson 1993). remaining withthose more than seeds viablefor yearsfive are for the SSB isclassified yearsfive orless, as short more than viable for a 1993).year (Thompson remain viableyear and seeds aorless seed persistent for banks when seeds longevity, classifiedRegarding can be seed SSBs seed as transient whe banks size lightseem and requirements, seed to be correlated (Milberg2000). al. et size seed small (Thompson 1993; Bowers Some traits, 2000). ofthese such as dispersal (Bowersgerminability 2000; B duringseed Baskin & a (e.g., theneed for post lightBowers1) requirements (Pons germination seed 1992; for 2) 2000), dormanc seeds that indicated the species plant of t on depends morphological sense,In physiological and traits. this it has seed been Article population which the occurs 1984).seed longevitythe (Reichman On other hand, varydensity can significantl seed and 1977; predationdispersal (Harper Mull MacMahon1996). & to due heterogeneous spatial longevity (Álvarez thesoil a in time remain for givenof period its and determine distribution, plant a whether forms it isnecessary SSB, a demonstratethat to viable strategy persistence annuala and (Harper species both perennial 1977). for seed soil importantThe bank (SSB) isan stagelifespan theplant in constitutes that Introduction
- Espino et al. etal. 2014). twoEspino canThe traits be first highly - maturation period; Murdoch & period; maturation Ellis1992) Murdoch low or y and populations among in among the microhabitats - temporal in production,seed seed fluctuations hat SSBs would be characterizedform by
When seedsviablein remain When - term persistent seedterm persistent
askin askin and3) 2014)
classified as long Thus, seed Thus,
seeds
banks, whilebanks,
density and density and
the soilthe To
remain
n
small know -
y
This article isprotected rights by All copyright. reserved. patterns,distribution seed inon studies SSBs cactus García 2012; (de Viana banks 1999;2005;Montaña Bowers 2000, & Cheib& Montiel 2003; do cactusspecies that SSBssome and form they short are 2011; soil seed seeds cactus Vázquez is species knowtheywhether (Rojascactus to bank seed soil a form & SosaRosas 2008). seedling emergfacilitate some growdocumented, species cactus withcavities, or rocks associated Even thoughnursecactus plant of facilitation establishment has been e availabilitynutrient canopy the under shade, provide and whichsubstantially soil temperature,provide protection minimum predators,against increase soil & diminish thecontrast SosaRosas 2008). plants betweenNurse themaximum early(Godínezimportant factor for establishment year (Godínez first germinate,very seeds the and most few of seedlingsemergent dosurvive not the In Americas. plantthese species, early establishment Accepted Article (Godínezvapotranspiration
Ortega An important An aspect understandingdynamics for the of early establishment a are diverseplant semiaridCacti arid family of and the to regions native -
Yanes 2000). The 2000).Yanes The banks (Bowers 2000; Rojas banks (Bowers 2000;
- Cano (seed size and positive and (seed suggest size that photoblastism) they form could Baes In thiset 2011). al. - - Alvarez et al. 2003). al. FacilitationveryAlvarez by plants isa nurse et Salgado et al. 2012
ence, survival growthetence, al. 2008; and (Peters
density and seed longevity seed density and (Álvarez species, onlyhas one simultaneously seed evaluated morphological and physiological and morphological - Alvarez et al. 2003; Munguía 2003; al. Alvarez et - Aréchiga Batis 2001;Flores al. & 2006, et sense,the on studies thetopicshowfew that ; Álvarez; - Espino et et al Espino - Alvarez et al. 20 al. Alvarez et
is a phenomenon, rare since - Rosas & & Sosa Rosas - term seedpersistent . 2014).. traits ofmost thetraits - Espino et al. etal. 2014). Espino 03;Munguía - Of all the all Of Aréchiga & Aréchiga
widely Munguía
2008). 2008). which
reduces reduces
-
-
and
in
This article isprotected rights by All copyright. reserved. and diameter cmcm 3 de Accepted soil30 random, samples each usingmicrohabitat afrom cylindrical (10 core metal (under microhabitats nurseand inplants bareAt each site,we areas). at took, determin We bankSeed Southern Andean Yungas Dirnestein & (Olson 2002). indiverse cacti mostthree ecoregions this for Dryprovince: High Monte Chaco, diversity (Ortega Argentina in study The in the wasSalta province, with conducted region the areaStudy Methods and Materials Articlethey produce. to speciesdetermineus whether cactus what and banks form seed soil sites? and and 3) isth What densityseed vary microenvironmentsor (nurse plant bare spatially among soil previousthe yearsviableuntil the remain in next reproductive event? Specifical bank. al. Baes et 2010 suggesttheyb) short a that wouldproduce Argentina. Previous studiesArgentinean(deon cactusspecies Viana 1999; distribution,seedstudying longevity seed density and northwestern in context, this cactusIn whether we soil evaluated species form seed banks
ed theseed distribution density and two in by samples soil collecting
ly, we address ly, Dothe 1) address we seeds following questions: produced
pth). A variablepth). A linear transectsnumber of 100 wereof m e longevity seed thesoil? in - Baes al. Baes et 2015). sitesselected 12 in located We
This informationThis - term persistent highestcactus
type of bank
will allow 2)
areas)
seed Ortega Does
in
and the ,
- This article isprotected rights by All copyright. reserved. v Acceptedfour species, in bags under nothem paper laboratory longer a than conditions week.for we seeds the fruiting season, extracted from ten speciesand per mature fruits spegazzinii terscheckii longevitySeed was onlyfor ( six evaluated species longevity Seed (germinated seedsseeds non and For b). each2010 species, abundance seed was theas determined number of viablewhen theirturgidconsidered embryoswhite(Ortega were and with stereoscopic longitudinallyobserving a and them microscope. was seeds atgerminated of evaluated the theend ArticleThe germination collected seeds, the wenot perform a did study ofthis aim was evaluate to collection.seed were and counted. identified soil each sample and extracted using theseeds sieves. metal theseed to prior dispersalperiod remain the least soil viablein could at for one samplingyear, the was to collectthe established required number of samples.
emergence ofthe as wasradicle defined viabilitygermination. the The non of , ) because therewere enough not availableseeds ) because all species. for
E.thionantha chambers 30 anddaysfor at 25°C a photoperiod 12/12 hof light/dark. oile bagsoile seeds containing100 were each under buried
We built We
theywere in placed community capacity determine thegermination analysis. of To it ,
Gymnocalycium saglionis from from Seed identification was out carried seeds
. In. thelaboratory,we the determined whether cactuswhether produced species bank, seed soil a - germinated viableseeds)/250 cm
collected Petri dishes with Petri dishes 1% agar and incubatedin in each of assay by them cutting Echinopsis atacamensisEchinopsis
,
G. schickendantzii To determineTo whether studied studied All the
using reference a site Seeds wereSeeds 3
-
extracted seedsextracted Baes Baes et al. . performed
s
woody volume of .
and Since the
For each For each ,
During E. G.
seeds
stored
viab
-
le This article isprotected rights by All copyright. reserved. Arg Córdoba, performed using InfostatsoftwareGrupo InfoStat. (version 2009, significant a indicated (Didifference Rienzo2002). etal. was DGC √x. addition, a means comparisontest usedIn multiple germinating seed and of (proportion viability) seeds were transformed microenvironments burial and among times. of in germinating differences the proportion seeds viabilityand seed and sites microenvironments. used thesame analysis We areas. wasbare ANOVA performedto in detect density differences seed T analysis Statistical Seed above. viabilitydetermined describedwas as f evaluate theirto germination viability and laboratory the under seeds bag withfrom (i.e., each canopy 100 under microenvironment 12, 24 and 36 months burial. buof each When i.e.,seeds, before burying (zero time), them burial seeds and of the exhumed after data in species cactus woodySelected that specieswerethe showed association those highest level with and thesamespecies, number of were seeds bags and in buried bare -
Acceptedtests were performedto evaluate differences seed in number between canopy Article ).
We determined thegermination viability proportion seed and We the of fresh entina). the
study (i.e., sites potential nurse potential nurse plants; In analyses, all the response rialwe timewas reached,
or or the soil All
to evaluateto the
analyses were Ortega
conditions described described conditions seed banks.
FCA when theANOVA -
between between Baes, unpubl. Baes, and bare and area)
-
using arcsine UNC, areas.
extracted a a extracted among among
probable variables
and
6, 6, This article isprotected rights by All copyright. reserved. the canopy under site. at Las Abritas ( interaction microenvironments site.For ( interaction saglionis microenvironments cactusfor of most the studied. species for in seeds of differences the number between microenvironment speciesNine site. presented seeds only underSignificant (Table 1). canopy seed density highest recorded was for with sitesspecies thegreatestnumber of atacamensis presentedseeds samples(50%) thesoil in ( corrugata verticillataQuiabentia boliviana the samples any thesubfamilyfor of species of ( Opuntioideae in thewere soil No (Table samples 1). were present seeds recorded thesoil in thesites, all weAcross but 32(62.5%) cactusspecies, recorded ofthem only 20 bankSeed Results Accepted Article aethiops Cereus E. rhodotricha E. No significant differences significant seed No in density were among recorded sites or
G. schickendantziiG. , significant, differences were the only detected microenvironment for , ). The same ). with same ofoccurred threespeciesThe the subfamily Cactoideae Opuntia anacantha
F F ,
= 4.06, = 3.23, E.terscheckii , , Echinopsis thelegonaEchinopsis G. saglionis G.
( F P P ,
= 4.18, = 4.18, Salmiopuntia salmianaSalmiopuntia
= 0.046). = highest 0.046). The thisdensityseed specieswas for the beingcanopy = under higher 0.042), at Las Abritas , significant differences were betweensignificant recorded , ,
G. saglionis saglionis G. ,
P , O.quimilo
G. schickendantziiG. = 0.043) and the microenvironmentfor Significantdifferences between G. spegazziniiG.
and ,
and
with seeds inwith (Table thesoil seeds 1). The O. schickendantziiO. in
Gymnocalycium pflanzii G. spegazziniiG. more than withmore than one site, ,
Tephrocactus weberi
and
under canopy,the Punillaunder at G. spegazziniiG. For , being the cactus the being
O. sulphurea O. Cumulop s were only recorded Gymnocalycium and
). (Table 1). (Table E. - Ten species Ten site untia
Tunilla
,
- site
found found
This article isprotected rights by All copyright. reserved. Acceptedmicroenvironment (microenvironment: microenvironment (microenvironment: significantlyinteraction germinating theproportion affected seeds of burial (Fig.of In 1F). 12 species, after In months of this burial. the viability seed 6 decreased from proportionburial,germination was6 significantlymonths at of higher decreasing recorded for progressive inburial. decrease This germination seed and viabilitywas 6decreased at months burial, with significant of a major decrease at 12 months of However, (Fig.B). viabilitytwo these seed burial species1A, the significantly for terscheckii wereviability ( only affected time by burial species Article seeds No allspecies. alwaysfor survived0.70 the ≥ 24 proportion The longevity Seed were no seeds samples thesoil because bare in areas found from comparisons among site the showed Punilla seed canopy highest density under for ( interaction their ( microenvironments
,
except for except for , the germination, significantlyproportion decreased af G. saglionis ofgerminated viable and seeds seeds
F - -
burial timeinteraction: buri = 6.09, E. thionantha E. F F F E. thionantha P. microsperma
= 13.22, = 13.22, = 75.08, = 6.19, = 6.19, al timeinteraction:al
and P
= 0.003) were= 0.003) onlyfor recorded G. spegazziniiG. P P P
= 0.014), a
, the , ofgerminatingproportion seeds seed and = 0.019; burial time: < 0.001; burial time: ,burial microenvironment, and time,
and F F E. albispinosa P
mong sites ( mong sites
= 6.75, = 20.12,
P = 0.006). F F atzero time were burial < and 0.0001) viability seed - F = 42.11, = 82.47, month populations were In In = 6.15, In G. schickendantziiG. G. spegazzinii E. atacamensis G.spegazzinii burial time. In this the species, ter ter 12 months P P P < 0.0001; < 0.0001; (Table1). = 0.003) and = 0.003) for their also performed performed In all . The . months and No , the , of of E. This article isprotected rights by All copyright. reserved. duringearly speciescan of onlythese occur establishment the autumn these some of havesince species end by mature fruits of the arid regionsof and semiarid northwest in Argentina. thesoil in subfamily samples, although they Opuntioideae conspicuous are seed distribution, cactus populations Á experimentallyexistence Álvarez 2013; (de Viana soil samples 1999; only subfamily traits on seed based Cactoideae (Ortega cactus The seed banks. formation of a bank was previously in samples, thesoil suggesting cactusspeciesseeds some that doseed soil form to According the results,60% of presented the evaluated cactusspecies viable Discussion zero obtained at burial seeand time for was seeds On under theother canopy. found the hand, seed highest after 6whileareas buried months, being thelowestfor proportion of germinatiproportion highest of Acceptedlvarez Article four A noteworthy result is that we s noteworthyA did not isthat result find Echinopsis atacamensis - - Espino et et al. Espino winter (e.g., studies have evaluated havestudies the seed existence evaluated cacti in of banks - Espino et al. al. while 2014), et Espino otherhave studies only their evaluated density and seed longevity.density seed and must be be integrativedone must using an including seed approach, Opuntia anacantha (2014), thedetermination ofthe presence ofa in bank seed soil (Bowers 2000, & 2005; García Cheib 2012). 2000, to(Bowers According Cano ng seeds was recorded at zero ng was seeds burial at andin time recorded (de Viana 1999) Viana species andsuggested (de for the of - Salgado al. 2012 et ds ds buried (Fig. 6 for months , O. quimilo eeds of cactuseeds of speciesofthe - Baes al. Baes et 2010 a, b). and This result wasThis not proposed for the columnar proposed for ; Holland; & Molina Tunilla the summer rainyi.e., the season, corrugata 1C). germinating germinating viability wasviability by analyzing expected ), so ), so the - or even inor Freaner Freaner So far, elements bare bare This article isprotected rights by All copyright. reserved. Accepted due toseeds almost null production. fruit cactus,in columnar soilbe could because samples of verya sense,In Cactoideae. this the absence of see in seeds somethe absence samplesof thesoil of cactus species for the vegetative (Ortega propagation their they lost have sexuality;cons clonalin thatsexualsuggested is cacti, rare reproduction a phenomenon salmiana suc reproduction, thesubfamilyspecies of recruit new Opuntioideae via individuals asexual variation constant spatial and extremelyor low production. fruit regions. the densityseed in opuntioid granivory Articlelow densitythat thesoil in iscaused recorded bank seed by seed highlevels of rodents,granivoryand ants For birds. of seed desert environments, bank dynamics is loss stronglybydue to seed affected seeddispersalwhether seed thespatial affects in distribution species. opuntioid and gravity, seeds the species are Field production. variation in observationsfruit the that indicate fruits some of seeddeposition patterns due to dispersers, causes followingThe probable of this could summer. finding Tayassu tajacu being activelybybeing consumed tayassuids ( Regarding and species the of and (Montiel & Montaña & 2003). (Montiel do notknow, predation affects how seed We in anthills. Inin opuntioid the cactus extensively by(e.g., ants consumed h h as ), animals with), animals vagility. great the third cause the third O. anacanthaO. Tephrocactus species - Baes & Gorostiague2013). couldBaes This also equently,a scalethey at local persist , show populations many temporal cactus either or , O. sulphurea in S Opuntia rastrera The latter seemsThe latter outhern Central Andessemiarid outhern and arid and 2) high level of seed2) highpredation level of O.quimilo ds of of ds Tunilla Tunilla Catagonus wagneri Future studies s studies Future O. sulphureaO. , Echinopsis O. schickendantziiO. , the to bythe fruits soil , fall genera it has been dem to consequence be a of be: 1) be:1) seed differential low or null availability of availability null low or of ), wh . thelegona Ithas Several cactus hould evaluate hould ich store ofstore most ich , Tayassu pecariTayassu been been , Salmiopuntia Salmiopuntia through subfamily , a, creeping because onstrated and 3) and 3) explain In This article isprotected rights by All copyright. reserved. conditions better and nutrients environmental than(e.g., temperature) bare areas Acceptedcouldprovide against plants Nurse predators, protection (Godínez microenvironment cactus the family, bydifferentialexplained the early in this establishment 2014). seed (Sánchezfunctioning as plants traps Secondary by streamingdispersal can seed occur wind and the frugivoresperch on primaryseedsThrough dispersal, could seed deposited be under (primary dispersal secondary and dispersal; Álvarez seed potenti schickendantzii two cactus microenvironments only for ( species four microenvironments.evaluated recorded seed in differences densityWe between Article onlyfound the samplescanopy soil under in potential nurse plantsboth of in or between microenvironments(i.e., canopy under in bare areas). and rain.Inaffectingpotential the thesameseed seed way,distribution variedthe because ofdifferentialbe productionamongpopul fruit years and the seed variedresults, density spatially cactus among populations. the et 2014) Espino al. and northwestern Argentina (de1999). Viana According our to not thosedo differ cactus recorded other from specie for by individuals very sexually few originated pollination since ofpopulations the failure The seed seed The densities in found the samples soil studied the different for species Cactus al nurseal plants. could pattern This be a consequence of - nurse associnurse plant y G. spegazziniiG. m (Godínez m - Alvarez et al. 2003; Munguía 2003; al. Alvarez et ), with density the ), always being ations have proven to be a common ations proven have be a phenomenonto - Alvarez et al. 2002;Álvarezal. Alvarez et - this self (Ortega Salas et et 2012; al. Salas - - incompatible species incompatible are formed Baes Gorostiague2013). Baes & E. rhodotricha s both ins both Mexico(Álvarez a greater availability greater a of - - Espino Rosas & & Sosa 2008). Rosas rain water,rain with nurse Álvarez differential seed differential - greater under the under greater Espino et al. etal. 2014). Espino ations, directly ations, et al. 2014). et 2014). al. nurseplants when , Seeds wereSeeds G. - Espino al. et Espino saglionis This could This , the G. - in This article isprotected rights by All copyright. reserved. primary(seed by dormancy), Álvarez proposed as schickendantzii wasgermination seeds. results foundrecently in obtained The collected for differingburial, species,the from remainingstudied In only withwere time, significant atburial 12 a decrease affected byburial. months of stellatus of action pathogenic fungi, has been as years three mortality ofseed two and at andhas been 2000) proposed for stellatus Stenocereus theseeds not since did survive schickendantzii atacamensis (i.e., agents biotic and physical agents). be explained byalso differential seeddistribution to due theeffectsseeof However,effects. plant show, our results as cactus (de Viana Argentina et 2001;al. recorded associated individuals plantswith species of n for nurse (Godínez Accepted schickendantziiG. Article According to results,( cactus to theAccording our six species studied species all In (Álvarez - Alvarez et al. 2003). In this context, In this greater 2003). al. cactus Alvarez proportion the of et , E.terscheckii could be explained bybe post could and - Espino et al. etal. 2014). Espino , G. spegazzinii except for , the greatestseed germination the was, at obtained of six months (Álvarez , E. thionantha E. - Espino et al. 2014) and 2014) et al. Espino E. thionantha E. 24 Ortega Echinopsis ) presented short ) presented months of burial. - described described the columnarcactusfor Baes, unpubl. data burial have occurred could through the , - Gymoncalycium saglionis maturity necessity for seed germinationmaturity seed for necessity , see, atacamensis atacamensis d seed and germination viability - Espino et et al. Espino - nurseassociations plant - in whichin the greatest seed This has been This term per Ferocactus wislizeni ) could result from (de (de Viana sistent banks seed Echinopsis (201 orthwestern demonstrated demonstrated for 4). , 1999). Cactus1999). G. d S. dispersal G. (Bowers (Bowers could nurse This article isprotected rights by All copyright. reserved. Accepted understandto how vary banks seed spatial bankcactusseed dynamics affect demographic a ofcycle.theas phase life sincestudies species (without most data support)field have very are understandingresults better for relevant population the and microenvironments populations.and among six least th At of species for the their that results Our & GarcíaCheib on afocused singlespecies(de 1999;Viana Bowers 2000; cactuswhether species soil ba form seed isthe firstThis comprehensive to studyat conducted evaluate, a community of hotspot cactusa diversity global scalethe (Ortega at Article longevity cactusspecies that many for speciesinnotall suggesting community a plant that nurse can act as cactus on seed germination. allelopathicinhibit potential effects The of potential likelynegative plant effects, nurse kill through thatallelopathic n potential significantly decreased12 after months of burial, significantlybeing lower factors (burialevaluated timeand microenvironment). ecological literature. As wasAs literature. ecological demonstrated,seed vary density can between Gymnocalycium In thepresentIn study,analyzedwe distribution, density seed seed seed and germination seed seedThe viabilityand of presence is common has previously more than much considered in been establishmentwas previouslyViana by et de al. proposed urse urse inplants than bare areas. stronglycactus that species do demonstrate 2012; Holland & 2012; Molina Holland genera, wegenera, that showed they short form Therefore, future Therefore, studies are distributed in distributed thesouthernare Central - Freaner 2013; Álvarez nks, since most nks,previous since studies most These results suggestThese results the - temporally as a consequence consequence of temporally a as behavior. In addition, it isnecessarybehavior. addition, In E. thionantha should what evaluateways in Both response - Baes et al. 2010 c, Baes 2010 et al. form seedform confirmingbanks, Montiel Montaña& 2003 notconsidered the - term seed - Espino et al. etal. 2014). Espino were by affected dynamics dynamics cactus of existence ofexistence (2001), variables plants. nurse nurse plants seeds and and seeds e banks. Ourbanks. under under Echinopsis have 2015). 2015). level, Andes, seed both both ; This article isprotected rights by All copyright. reserved. Accepted New(2005) Bowers transient J.E. or persistent for evidence Does(2000) Bowers J.E. C.C., BaskinBaskin J.M.(2014) HuntD. (2000) Barthlott Seed W., Álvarez References Article to scholarship Lindow Lucía FONCYTNo. (Grant 01149), No. 1492) (Grant by and FONCYTdoctoral a workmanuscript. This (GrantNo. wasby CIUNSalta supported Frizza authors N. thank withThe assistance theEnglishversion for of the Acknowledgements ofcactusdynamics species. variation longevity of seeds.longevity of the columnarcactusin Sonoran desert cacti. desert Sonoran Arid Journal of Environments dormancygermination and PlantResearch Succulent - Espino R., Godínez R., Espino s in annual seed annual productions in and how this Seed Research Science Ferocactus Ferocactus wislizenii - - The SouthwesternThe Naturalist Alvarez H., de la Torre la Alvarez de H., López. Stenocereus stellatus Stenocereus , Seeds. Seeds. . Academic . Press, US. 5 - diversity in the Cactaceae:diversity the subfamily in , 49. , 45 , 197 Ecology, - 205. have a betweenhave a biogeography, and evolution biogeography, evolution and of , affects the early establishment 24 - : Almaráz R. (2014) Seed banking Seed (2014) Almaráz R. distribution, density distribution, , 315 , 50 - 320. seed banks three in , 482, - 2060), CONICET year seedbank? - 487. Cactoideae. Cactoideae. and This article isprotected rights by All copyright. reserved. AcceptedGodínez Jurado J., A. EffectFlores E., (2006) lightArredondo onof germination ofseeds of Casanoves Guzmán A.W., Di Rienzo A J.A., F. multiple (2002) A.A.(2003) gynodioecy Cocucci Díaz Functional L., in M.L., Viana de Sühring Manly S., (2001) Application B.F.J. Article M.L. Viana (1999) de seed productionand Seed bank of A.L., Cheib García Longevity(2012) Q.S. ecologygermination and seeds of of Cano - Salgado a tree cactus tree a pollinated by plant. nurse study to of association the northwestern in (Cactaceae) Argentina. Research Science Seed Cactaceae speciesendemic high from y temporal región una en Pérez tetetzo the in population dispersers dynamics thecolumnarcactus of 149 Chihuahuan Desert,Cactaceae from the México. Biological Agricultural, Environmental and on thedistributionbased ofthe rootnode distance of binarya tree. - Alvarez Valiente H., - 155. – . Rodríguez Ecology A. . , Zavala, Revista Mexicana Mexicana BiodiversidadRevista de Plant Ecology Plant semiárida del semiárida variación del patrones trópico mexicano: de espacial , 83 P. (2012) (2012) P. - Hurtado , 2617 , - Banuet RojasA., , 22 - , Trichocereus pasacana bees and hummingbirds.bees and 2629. 156 , 45, Composición y banco abundancia del de semillas J.A., , 193, - 53. Orozco - 197. - altitude in sites so Tropical Ecology - - Martínez A. (2002) Martínez(2002) A. Segovia Statistics , 83,437, Opuntia Opuntia quimilo Seed Research Science Seed A., A., Trichocereus pasacana (Cactaceae) , Plant ofrandomization 7 Valverde , 129 - - 446. , comparisons uth Biology 40 - 142. - , 79 The role role ofThe eastern Brazil. Neobuxbaumia - Valdés with potential with potential - (Cactaceae), (Cactaceae), 84. , 5 Journal of , 1 methods method method - M.T., M.T., 9. seed , 16 , This article isprotected rights by All copyright. reserved. Accepted A.J., Murdoch Ellis R.H.(1992) Longevity,vi Munguía J.A.FactorsMacMahon (1996) spatial determiningMull seed J.F., the variability of S.,Montaña Montiel C. bank ofSeed (2003) cactusthe desert dynamics ArticleMilberg P., J.N., Molina Holland J. Harper Godínez densities in a shrub a in densities 248. rastrera Research light dependent on for small than germination Science granivory on cactusrecruitment. banks seed and Cactaceae. CABI Publishing, UK. CABI (ed). leucocephalus woodyand rocky therecruitmentof the on plants cavities Arid Environments - - Alvarez H., Valverde T., Ortega Alvarez T., Valverde H., L. (1977) Rosas M.A., Nurse (2008) M.A., vs.Sosa V.J. plant Rosas nurse effects objects: of Andersson (2000) Andersson L., K. Thompson Large Seeds: Seeds: theregeneration ecology of in plantcommunities , in twoin habit 24 , 10 , 1053 , Botanical Botanical Review Population of biology plants , 99 ‐ Freaner Hierarchical F.(2013) rainfall, effects nurse plants, of columnar cactus. - 104. - , 1061. - 32 ats from ats the from Chihuahuan Desert. steppethe role ecosystem: of ants. harvester , 181 - 192. , 69 Annals ofAnnals Botany , 173 - Baes Demographic(2003) the P. trends in ability and dormancy.ability and - 203. . Academic Press, UK. Academic Press, - seeded ones. ones. seeded - seeded species less seeded are Journal of Vegetation , 101 PlantEcology , 175 Pilocereus In: Fenner, M. Fenner, In: - Seed Science Seed 185. , pp pp 193, Journal of Opuntia , 166 - 229. , 241 - This article isprotected rights by All copyright. reserved. AcceptedOrtega Ortega Ortega ArticleOrtega Orozco Dinerstein D.M., (2002) Olson Global E. The global Priority200: for ecoregions 342. toresponses light? Rojas Environments 25 speciesevaluation of northwestern from Argentina. of Annals to seed relation dormancy in A.,C.C.(2007) Buen Baskin J.M., anatomyBaskin Seed water and in uptake conservation. de la la Sociedadde Argentina de Botánica de diversidadPatrones políticas y pa prioridades C., Sosa Curti R.N.,L.T., (2015) Juárez A. LaCactaceae enfamilia Argentina: Galíndez Bravo S., López G., biotechnology cactus family. Godínez - - - - - Baes G Baes P., SühringBaes P., AparicioBaes P., AparicioBaes P., (2010a)M., Galíndez G. Vivipary cactus family:an the in Segovia Márquez A., - Aréchiga M. (2010b) Are M.(2010b) Aréchiga cactusgrowthto related germination forms - Alvarez H. (2010c) Chapter DiversityAlvarez 8: (2010c) H. conservation in the and Botany odínez , , pp 157 Annals ofAnnals the Missouri Botani In: Ramawat, (ed.)In: K.G. 74 , , 1359 99 - S., SajamaJ.,S., Sotola E., Alonso - GonzálezGalíndez del Fueyo P., M., G., Sühring S., A testusing A Alvarez H., Sajama Gorostiague P., SühringJ., Alvarez Sajama H., S., , 581 - - 173, Springer, Germany. Springer, 173, Guzmán J.,Sánchez Guzmán - 1361. - 592. Opuntia tomentosaOpuntia - Spahr D., Alonso D., Spahr Echinopsis , Desert plants: biology and Desertbiology and plants: 50 , 71 cal Garden species. - Coronado M.E.,de Gamboa Coronado - 78. - Pedano M.,Lindow Pedano (Cactaceae,Opuntioideae). ra su conservación. - Pedano M., Bravo S., Acta Acta Oecologica , Journal of Arid 89 , 199, - 224. - López López Boletín Boletín , 36 , 339, - This article isprotected rights by All copyright. reserved. Accepted ( E.W. Schupp Sánchez Rojas Rojas O.J.(1984). Reichman andtemporalvariation Spatial seed of indistribution Article (1992) Pons T.L. Se E.M., Peters Ortega - - el suelo? suelo? el soils. Desert communities. plant in regeneration 72 ( plantsin nurse determining anddistribution the cacti establishmentof globose 785 clonalcactus the recruitment. recruitment. 707 e species dispersal adapted germination and Desert for during floods: Arid Journal of Environments Aréchiga M., Vázquez M., Aréchiga Batis M., Aréchiga Las(2001) de semillas cactáceas¿forman A. en … bancos - Mammillaria Baes Gorostiague(2013)Baes P., P. Extremely reproduction sexual reduced in xperimental evidence two in - , 593 Salas J., Jurado Jurado FloresJ., E., J., Salas Estrada - - 791. 711. Martorell Ezcurra (2008) C., are E. rocks more importantNurse than - 1995) Seed 1995) 601. Cactáceas Mexicanas y Suculentas American Journal BotanyAmerican of Journal ) in the the Tehuacán) inValley, Mexico. Journal Journal of Biogeography ed to light. responses In: M.(ed.). Fenner, Echinopsis thelegona Echinopsis - seedling conflicts, choiceand habitat patterns of plant - Yanes C. (2000) germination: C.seed Yanes Cactus review.a , Astrophytum 44 ; 85 CABI Publishing, CABI UK. - 104. , 11 . Plant Systematics Evolution and , - , 1 82 Castillón E., Muro Castillón species (Cactaceae). (Cactaceae). species - , 399 11. , 46 Journal of Journal of Arid Environments - , 76 409. - 82. Seeds:the ecology - Péreza G. Péreza G. Flora Sonoran , (2012) (2012) 207 , 299 , , of of , This article isprotected rights by All copyright. reserved. Accepted letters indicate differencesDifferent significant ( Gymnocalycium saglionis areas) bare for (0, 6 each times and 12the months)(under in of microenvironments 1. Figure under canopybetween bare areas and for Articlespeciesand site, microenvironment. Different indicate significant letters differences 1. Table Captions (1993) K. Thompson in Persistence In:Hendry, soil. Grime,G.A.F.(eds). & J.P. Chapman and Hall, UK. Hall, and Chapman comparative in Methods ecology, laboratory plant man a Number Number viableseeds(meanSD) ± of samples soil (250cm in Seed germination (□) germination viabilitySeed andseed EE) ± at (■) (mean Echinopsis atacamensis (D) , G. spegazziniiG. , (A) each species ( , E. terscheckii E. , (E), and P < 0.05). G. schickendantzii P (B), < 0.05). ual E. , pp, 199 thionantha thionantha canopy and canopy and different burial different 3 ) each for (F). - 202. (C), This article isprotected rights by All copyright. reserved. Accepted Article(2006). S1. Table Supporting information Cactus species thestudied in registered sites . Taxonomy follows Hunt Hunt This article isprotected rights by All copyright. reserved. Accepted Piedra Casa de ElAlgarrobal Article Azules Peñas El Galpón La Pedrera Site areas for each species microenvironment. Different letters indicate significant differences between under canopy andbare Table 1 . Number of viable seeds (mean SD) ± in soil samples (250 cm ( P Stetsonia coryne Harrisia pomanensis C. hankeanus C. baumannii G. schickendantzii Gymnocalycium saglionis E. terscheckii E. albispinosa Cleistocactus baumannii E. albispinosa E. rhodotricha Echinopsis terscheckii Species C. baumannii E. terscheckii C. smaragdiflorus E. rhodotricha < 0.05). 1.38±2.84 0.76±2.18 0.84 1.09±2.42 1.1±3.38 Under canopy 0.43±1.15 0.6±1.43 0.68±1.65 1.4±4.87 0.22±0.47 0.45±1.44 1.32±3.21 1.65±3.64 0.56±1.32 0.64±1.51 1.84±3.95 ± 1.97 A A A A A A A A A A A A A A 3 ) for each for ) site, species and 0.46±1.55 0 0 0.09±0.52 0.56±2.11 areasBare 0.33±1.27 0.76±3.21 0.14±0.44 0.35±0.84 0.41±0.8 0.1±0.57 0.47±1.47 0.38±1.19 0.55±1.81 0.57±1.71 0.7±1.82 A A A A B A A A A A A A A A This article isprotected rights by All copyright. reserved. Accepted Seclantás 2 LosCardones Seclantás 1 Punilla Article LasAbritas Sunchales G. spegazzinii E. atacamensis P. microsperma G. spegazzinii E. atacamensis E. leucantha E. aurea G. schickendantzii G. saglionis E. terscheckii E. ancistrophora Parodia microsperma G. schickendantzii G. saglionis C. smaragdiflorus E. atacamensis Denmoza rhodacantha E. atacamensis E. haemathantha 1.8±3.65 2.22±3.81 1.88±3.83 2.88± 9.23 1.98±6.35 0.74±2.14 0.72 ± 2.51 1.24 ± 3.61 1±3.71 0.97 ± 0.97 ± 2.76 0.31 ± 1.24 0.55 ± 2.04 0.4±1.24 0.44±1.41 1.18±4.62 0.4±1.41 18.35±39.44 0.35±1.34 0.68±1.81 A A A A A A A A A 0.61±2.37 0.29±0.91 0.21±0.84 0.36 ± 1.15 0.49 ± 1.69 0.21±1.14 0 0 0.71±2.27 0 0 0 0 0.6±2.36 0.17±0.91 0 0.46±1.27 0.38±1.01 0 A A B B A A A B A This article isprotected rights by All copyright. reserved. Accepted Article Yacochuya E. atacamensis G. spegazzinii G. saglionis G. spegazzinii P. aureicentra E. thionantha 0.37 ± 0.37 ± 1.17 0.55 ± 1.58 0.54 ± 1.3 0.49 ± 1.87 0.17 ± 0.63 0.28 ± 1.06 A A A A A 0.46 ± 0.46 ± 1.52 0 0.68 ± 2.29 0.23 ± 0.9 0.780.2 ± 0.36 ± 1.13 A A A A A This article isprotected rights by All copyright. reserved. Accepted Article