Phytocoenologia 33 (1) 13 28 Berlin Stuttgart March 18 2003

Plant succession in abandoned gypsum quarries inSE Spain

by Juan Francisco Mota Ana Jose So la ElDaggeras David Dana andMarDaggera Luisa Jim enez-Sanchez AlmerDaggera

with 6 figures and 4 tables

Abstract Gypsum outcrops harbour a considerable number of rare species the presenceof which is restricted to these soils By the rarity and richness of their flora gypsum soilsof AlmerDaggera Province (SE Spain) are the most valuable in Spain from a conservation view-point whereas at the same time the territory is being intensively exploited by quarryingand holds the most important production of gypsum rocks in Europe It was hence con-sidered a priority to investigate the recovery patterns of gypsophilous species after quar-ries abandonment in order to seek for information that can help to develop restorationplans with an ecological basis For this aim chronosequences were established and thecolonising flora (presence and abundance) in each successional state was recorded andcompared to the non-disturbed communities Data were mainly analysed by means ofFrequency Diagrams and Multivariate Methods Dendrograms resulting from the ClusterAnalyses showed the existence of two well-defined groups of species that differed in theircolonisation power One of the groups harboured Gypsophila struthium subsp struthiumthe dominant gypsophyte in the early states (in quarries abandoned up to 25 years ago)which coexists with other less abundant ruderal species The other group was character-ised by the presence of the remaining gypsophytes such as the endemisms Teucriumturredanum or Helianthemum alypoides which show a low colonisation ability and ap-pear in the last stages (mainly in quarries abandoned more than 30 35 years ago) Ordina-tion Analyses separated the samples taken from the unaltered scrub from the otherswhich indicates that although there is a clear tendency towards the recovery of gypsumsoils by the gypsophytes of the area the primary succession does not lead to the re-establishment of the relative abundances of all the original species in the interval of timeconsidered

Keywords primary succession restoration ecology gypsophytes multivariate analysis

Nomenclature Taxonomic nomenclature follows Castroviejo et al (1990 1993 19971999) for the published families and Tutin et al (1964 1980) for the remaining taxaexcept for Launaea fragilis (Asso) Pau (Lo pez-Go nzalez 1980) Table 1 shows the scien-tific name and abbreviation used for each species throughout this work

Introduction

Gypsum outcrops are widely distributed around the World and generallyappear in areas subjected to dry or semiarid climate (Watso n 1979 Par-sons 1976) Many authors have reported the restriction of the vascular

DOI 1011270340-269X20030033-0013 0340-269X030033-0013 $ 4002003 Gebruumlder Borntraeger D-14129 Berlin middot D-70176 Stuttgart

14 J F Mota et al

Table 1 Scientific name and abbreviation of the studied species

Species Abbreviation

Andryala ragusina And_ragAnthyllis terniflora Ant_terArtemisia barrelieri Art_barArtemisia campestris subsp glutinosa Art_gluAsphodelus cerasiferus Asp_cerAsparagus acutifolius Asp_acuAsparagus horridus Asp_horCoris hispanica Cor_hisDiplotaxis lagascana Dip_lagDittrichia viscosa Dit_visElaeoselinum tenuifolium Ela_tenEryngium campestre Ery_camFagonia cretica Fag_creFrankenia thymifolia Fra_thyFumana thymifolia Fum_thyGypsophila struthium subsp struthium Gyp_strHelianthemum almeriense Hel_almHelianthemum alypoides Hel_alyHelianthemum squamatum Hel_squHelianthemum syriacum Hel_syrHelichrysum italicum subsp serotinum Hel_serHerniaria fontanesii subsp almeriana Her_almLaunaea fragilis Lau_fraLaunaea lanifera Lau_lanLepidium subulatum Lep_subOnonis tridentata Ono_triPiptatherum miliaceum Pip_milPlantago albicans Pla_albRetama sphaerocarpa Ret_sphSantolina viscosa San_visSedum gypsicola Sed_gypSedum sediforme Sed_sedStipa parviflora Sti_parStipa tenacissima Sti_tenTeucrium turredanum Teu_turThymelaea hirsuta Thy_hirThymus hyemalis Thy_hye

plants to this type of substrate henceforth lsquogypsophytesrsquo (Emerso n 1935Cambell amp Cambell 1938 Jo hnsto n 1941 Meyer 1986) However andby the moment there is not a definitive explanation of this extreme bondbetween plant and soil properties neither of the role of gypsum crusts asrefuges or centres of plant speciation (Duvigneaud amp Deneayer-De Smet1966 1968 Meyer 1986 Powell amp Turner 1977)

In the Iberian Peninsula most of the studies have been devoted to thedescription of plant communities from a phytosociological viewpoint (e g

15Plant succession in abandoned gypsum quarries

Rivas-Go day et al 1956 Braun-Blanq uet amp Bo lo s 1958 Rivas-Go day amp Esteve 1965 Rivas-Go day amp Rivas-Martinez 1967 Rivas-Martinez amp Co sta 1970 Lo idi amp Co sta 1997) More recently someother contributions have focussed on the ecological and physiological as-pects (e g Escudero et al 1997 1999 2000a 2000b Merlo et al 19971998 2000 Dana 2000) and on the importance of gypsum soils in the frameof conservation strategies (Cerrillo et al 2002) since many of their speciesare protected at regional national and international levels (Pinto s amp Ro -driguez-Hiraldo 1994 The Red Book of Go mez-Campo (1987) lists12 gypsophytes in Spain Centaurea pinnata Helianthemum alypoides Li-monium album L aragonensis Narcissus tortifolius Nepeta beltranii San-tolina viscosa Teucrium lepicephalum T libanitis T turredanum Thymuslacaitae and T moroderi Nine of them are also included under some of thethreaten category of the IUCN in the recent Red List of Spanish VascularFlora (VVAA 2000) whereas the local endemisms Centaurea pinnataTeucrium lepicephalum T turredanum and Helianthemum alypoides arepriority species for the European Habitats Directive (Ano nymo us 19921997) which also consider the gypsum outgrops and their communities aspriority areas for conservation

The most valuable territories for the conservation of the Iberian gypsumflora are the southeastern lands in the province of AlmerDaggera (Dana 2000)and among these the outcrops of Sorbas-Los Castanos and Tabernas (Cer-rillo et al 2002) These areas harbour one of the worthiest karsts systemson gypsum soils worldwide (Calafo rra amp Pulido -Bo sch 1997) Al-though Sorbas outcrops are partially protected as Natural Area by the An-dalusian Government they are greatly threatened by the intense extractionof gypsum the area is the first European producer of gypsum mineral which causes a dramatic environmental and landscape impact (Fig 1) Theseactivities destroy the karsts systems and alter the rich and original floraof these habitats endangering the further existence of the gypsophilouscommunities

Given these precedents it was considered a priority to study how thesepractices affect the species composition of the pre-existing vascular plantcommunities and to provide the necessary information for the further de-velopment of restoration plans with an ecological basis To achieve this aimin this work the pattern of primary succession is investigated at specieslevel

Study area

The study area is located in the province of AlmerDaggera (SE of the IberianPeninsula) in the Tabernas-Sorbas intermountain basin (Fig 2) which wasformed by evaporates filling during the Messinian Salinity Crisis It is sub-jected to a Mediterranean Macrobioclimate (Rivas-Martinez 1996) andcharacterised by at least two arid months in summer (Fig 3)

Sampled sites (abandoned quarries) were located in Venta de los Yesos(close to Tabernas) and Sorbas-Los Castanos (Fig 2) In both enclaves gyp-

16 J F Mota et al

Fig 1 Abandoned gypsum quarry in Venta de los Yesos

Fig 2 Location of the study areas

17Plant succession in abandoned gypsum quarries

Fig 3 Ombrothermic diagrams from the climatic stations of ldquoLos Gallardosrdquo and ldquoTa-bernasrdquo

sophilous plant communities are dominated by short scrub species with40 in cover whereas the therophytes are scarce and mainly dwell themicrotopographic basins which are formed by deposits of fine materials(Lazaro 1984) The rest of soil is covered by cryptogams a stratum thatcan cover up to 90 of the soil gypsum crusts Two gypsophilous scrub

18 J F Mota et al

Table 2 General distribution of the gypsophytes and their occurrence at the study sitesSorbas and Venta de los Yesos

Gypsophytes Sorbas-Los Venta de DistributionCastanos los Yesos

Coris hispanica X X LocalFrankenia thymifolia ndash X WideGypsophila struthium s str X X WideHelianthemum alypoides X ndash LocalHelianthemum squamatum X X WideHelianthemum syriacum X X WideLepidium subulatum ndash X WideOnonis tridentata X ndash WideSantolina viscosa X X LocalSedum gypsicola X X WideTeucrium turredanum X ndash Local

communities dwell the outcrops Santolino viscosae-Gypsophiletumstruthi i Rivas-Goday amp Esteve 1965 in Venta de los Yesos and Helian-themo alypoidis-Gypsophiletum struthi i (Rivas-Go day amp Esteve1965) Alcaraz et al 1989 in Sorbas both of them belonging to the OrderGypsophil etal ia Bellot amp Rivas Goday in Rivas Goday et al 1997 Thefloristic composition of the two localities is shown in Table 2

Methods

Sampling methods

To approach the problem of the study of successional patterns it was em-ployed the theoretical concept of chronosequence i e the use of differentsuccession states which chronologically ordered give us a sequence of thedynamic of the species and plant communities in a defined interval of timeTwo sets (one per locality Tabernas and Sorbas) of quarries abandoned atdifferent moments in the last 50 years were employed Three successionalstages were consideredStage I (initial) which includes quarries that were abandoned 8ndash 12 yearsagoStage II (or medium) which includes quarries that were abandoned 20ndash 30years agoStage III (or advanced succession) which includes quarries that were aban-doned between 35ndash 70 years ago

We have also considered the scrubland non-disturbed by the quarryingin order to use it as an ecological station of reference or as the potentialnatural vegetation (White amp Walker 1997) Table 2 shows the gypso-phytes of this stadium in each site and their distribution

It must be indicated that the intervals are not continuous since theybelong to different waves of quarries opening by private companies

19Plant succession in abandoned gypsum quarries

Table 3 Study site characteristics location abbreviation time since last intervention sam-pling intensity VY (Venta de los Yesos) SO (Sorbas) FI (stage I abandoned 8ndash 12 yearsago) FII (stage II abandoned 20ndash 30 years ago) FIII (stage III abandoned up to 35 yearsago) M (unaltered shrubland or ldquomatorralrdquo)

Localities Sites UTM Abbreviation Years since last Number ofhuman intervention samplings

(aprox)

Venta de los Los YesosWG30S6204 VYFIndash VYFII 10 20 40 10

YesosWG30S6304 VYM Unknown 10

Cerrillo Blanco WG30S6203 VYFIII 35 10

Penon DDaggeraz WG30S8004 SOFI 10 5

HuelDagger WG30S8003 SOFI 8 5

Los Molinos WG30S8105 SOM Unknown 5

WG30S8309 SOM Unknown 5

Cerron WG30S8310 SOFIIndash SOFIII 25 40 5 3WG30S8409 SOFIIndash SOFIII 25 40 5 3WG30S8410 SOFIIndash SOFIII 25 40 5 2

Sorbas-Los Castanos

Species presence and coverage values were recorded at random in 5 m times5 m quadrats Due to small variations in quarries size the number of sam-ples was slightly variable too although at least three samples were taken ateach site Thirty-three samples were collected from eight quarries in Sorbasand 60 quadrats sampled in six quarries in Venta de los Yesos In additiontwenty quadrats from the unaltered scrubland were sampled near the aban-doned quarries (ten per locality) In order to avoid the problem of pseudo-replication each sample was collected far enough from each other Table 3shows complementary methodological details

Data analysis

In order to analyse the behaviour of the species involved in the plant suc-cession in quarries and to detect groups of taxa that follow the same succes-sional pattern species abundance times successional state matrixes were con-structed and subjected to classification (Cluster Analysis) and ordinationanalyses (Correspondence Analysis) by means of the statistical packagePC-ORD (McCune amp Meffo rd 1997) This procedure also allowed toinvestigate whether the successional trends could lead to the recuperationof species composition and relative abundances recorded in the unalteredscrublands considered here as the potential vegetation

For classification procedures Sorensen Jaccard and Kulczynski coeffi-cients were used to build up the similarity matrix (Po dani 1994) and dif-ferent linking strategies attempted (Nearest Neighbour Farthest Neigh-

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

14 J F Mota et al

Table 1 Scientific name and abbreviation of the studied species

Species Abbreviation

Andryala ragusina And_ragAnthyllis terniflora Ant_terArtemisia barrelieri Art_barArtemisia campestris subsp glutinosa Art_gluAsphodelus cerasiferus Asp_cerAsparagus acutifolius Asp_acuAsparagus horridus Asp_horCoris hispanica Cor_hisDiplotaxis lagascana Dip_lagDittrichia viscosa Dit_visElaeoselinum tenuifolium Ela_tenEryngium campestre Ery_camFagonia cretica Fag_creFrankenia thymifolia Fra_thyFumana thymifolia Fum_thyGypsophila struthium subsp struthium Gyp_strHelianthemum almeriense Hel_almHelianthemum alypoides Hel_alyHelianthemum squamatum Hel_squHelianthemum syriacum Hel_syrHelichrysum italicum subsp serotinum Hel_serHerniaria fontanesii subsp almeriana Her_almLaunaea fragilis Lau_fraLaunaea lanifera Lau_lanLepidium subulatum Lep_subOnonis tridentata Ono_triPiptatherum miliaceum Pip_milPlantago albicans Pla_albRetama sphaerocarpa Ret_sphSantolina viscosa San_visSedum gypsicola Sed_gypSedum sediforme Sed_sedStipa parviflora Sti_parStipa tenacissima Sti_tenTeucrium turredanum Teu_turThymelaea hirsuta Thy_hirThymus hyemalis Thy_hye

plants to this type of substrate henceforth lsquogypsophytesrsquo (Emerso n 1935Cambell amp Cambell 1938 Jo hnsto n 1941 Meyer 1986) However andby the moment there is not a definitive explanation of this extreme bondbetween plant and soil properties neither of the role of gypsum crusts asrefuges or centres of plant speciation (Duvigneaud amp Deneayer-De Smet1966 1968 Meyer 1986 Powell amp Turner 1977)

In the Iberian Peninsula most of the studies have been devoted to thedescription of plant communities from a phytosociological viewpoint (e g

15Plant succession in abandoned gypsum quarries

Rivas-Go day et al 1956 Braun-Blanq uet amp Bo lo s 1958 Rivas-Go day amp Esteve 1965 Rivas-Go day amp Rivas-Martinez 1967 Rivas-Martinez amp Co sta 1970 Lo idi amp Co sta 1997) More recently someother contributions have focussed on the ecological and physiological as-pects (e g Escudero et al 1997 1999 2000a 2000b Merlo et al 19971998 2000 Dana 2000) and on the importance of gypsum soils in the frameof conservation strategies (Cerrillo et al 2002) since many of their speciesare protected at regional national and international levels (Pinto s amp Ro -driguez-Hiraldo 1994 The Red Book of Go mez-Campo (1987) lists12 gypsophytes in Spain Centaurea pinnata Helianthemum alypoides Li-monium album L aragonensis Narcissus tortifolius Nepeta beltranii San-tolina viscosa Teucrium lepicephalum T libanitis T turredanum Thymuslacaitae and T moroderi Nine of them are also included under some of thethreaten category of the IUCN in the recent Red List of Spanish VascularFlora (VVAA 2000) whereas the local endemisms Centaurea pinnataTeucrium lepicephalum T turredanum and Helianthemum alypoides arepriority species for the European Habitats Directive (Ano nymo us 19921997) which also consider the gypsum outgrops and their communities aspriority areas for conservation

The most valuable territories for the conservation of the Iberian gypsumflora are the southeastern lands in the province of AlmerDaggera (Dana 2000)and among these the outcrops of Sorbas-Los Castanos and Tabernas (Cer-rillo et al 2002) These areas harbour one of the worthiest karsts systemson gypsum soils worldwide (Calafo rra amp Pulido -Bo sch 1997) Al-though Sorbas outcrops are partially protected as Natural Area by the An-dalusian Government they are greatly threatened by the intense extractionof gypsum the area is the first European producer of gypsum mineral which causes a dramatic environmental and landscape impact (Fig 1) Theseactivities destroy the karsts systems and alter the rich and original floraof these habitats endangering the further existence of the gypsophilouscommunities

Given these precedents it was considered a priority to study how thesepractices affect the species composition of the pre-existing vascular plantcommunities and to provide the necessary information for the further de-velopment of restoration plans with an ecological basis To achieve this aimin this work the pattern of primary succession is investigated at specieslevel

Study area

The study area is located in the province of AlmerDaggera (SE of the IberianPeninsula) in the Tabernas-Sorbas intermountain basin (Fig 2) which wasformed by evaporates filling during the Messinian Salinity Crisis It is sub-jected to a Mediterranean Macrobioclimate (Rivas-Martinez 1996) andcharacterised by at least two arid months in summer (Fig 3)

Sampled sites (abandoned quarries) were located in Venta de los Yesos(close to Tabernas) and Sorbas-Los Castanos (Fig 2) In both enclaves gyp-

16 J F Mota et al

Fig 1 Abandoned gypsum quarry in Venta de los Yesos

Fig 2 Location of the study areas

17Plant succession in abandoned gypsum quarries

Fig 3 Ombrothermic diagrams from the climatic stations of ldquoLos Gallardosrdquo and ldquoTa-bernasrdquo

sophilous plant communities are dominated by short scrub species with40 in cover whereas the therophytes are scarce and mainly dwell themicrotopographic basins which are formed by deposits of fine materials(Lazaro 1984) The rest of soil is covered by cryptogams a stratum thatcan cover up to 90 of the soil gypsum crusts Two gypsophilous scrub

18 J F Mota et al

Table 2 General distribution of the gypsophytes and their occurrence at the study sitesSorbas and Venta de los Yesos

Gypsophytes Sorbas-Los Venta de DistributionCastanos los Yesos

Coris hispanica X X LocalFrankenia thymifolia ndash X WideGypsophila struthium s str X X WideHelianthemum alypoides X ndash LocalHelianthemum squamatum X X WideHelianthemum syriacum X X WideLepidium subulatum ndash X WideOnonis tridentata X ndash WideSantolina viscosa X X LocalSedum gypsicola X X WideTeucrium turredanum X ndash Local

communities dwell the outcrops Santolino viscosae-Gypsophiletumstruthi i Rivas-Goday amp Esteve 1965 in Venta de los Yesos and Helian-themo alypoidis-Gypsophiletum struthi i (Rivas-Go day amp Esteve1965) Alcaraz et al 1989 in Sorbas both of them belonging to the OrderGypsophil etal ia Bellot amp Rivas Goday in Rivas Goday et al 1997 Thefloristic composition of the two localities is shown in Table 2

Methods

Sampling methods

To approach the problem of the study of successional patterns it was em-ployed the theoretical concept of chronosequence i e the use of differentsuccession states which chronologically ordered give us a sequence of thedynamic of the species and plant communities in a defined interval of timeTwo sets (one per locality Tabernas and Sorbas) of quarries abandoned atdifferent moments in the last 50 years were employed Three successionalstages were consideredStage I (initial) which includes quarries that were abandoned 8ndash 12 yearsagoStage II (or medium) which includes quarries that were abandoned 20ndash 30years agoStage III (or advanced succession) which includes quarries that were aban-doned between 35ndash 70 years ago

We have also considered the scrubland non-disturbed by the quarryingin order to use it as an ecological station of reference or as the potentialnatural vegetation (White amp Walker 1997) Table 2 shows the gypso-phytes of this stadium in each site and their distribution

It must be indicated that the intervals are not continuous since theybelong to different waves of quarries opening by private companies

19Plant succession in abandoned gypsum quarries

Table 3 Study site characteristics location abbreviation time since last intervention sam-pling intensity VY (Venta de los Yesos) SO (Sorbas) FI (stage I abandoned 8ndash 12 yearsago) FII (stage II abandoned 20ndash 30 years ago) FIII (stage III abandoned up to 35 yearsago) M (unaltered shrubland or ldquomatorralrdquo)

Localities Sites UTM Abbreviation Years since last Number ofhuman intervention samplings

(aprox)

Venta de los Los YesosWG30S6204 VYFIndash VYFII 10 20 40 10

YesosWG30S6304 VYM Unknown 10

Cerrillo Blanco WG30S6203 VYFIII 35 10

Penon DDaggeraz WG30S8004 SOFI 10 5

HuelDagger WG30S8003 SOFI 8 5

Los Molinos WG30S8105 SOM Unknown 5

WG30S8309 SOM Unknown 5

Cerron WG30S8310 SOFIIndash SOFIII 25 40 5 3WG30S8409 SOFIIndash SOFIII 25 40 5 3WG30S8410 SOFIIndash SOFIII 25 40 5 2

Sorbas-Los Castanos

Species presence and coverage values were recorded at random in 5 m times5 m quadrats Due to small variations in quarries size the number of sam-ples was slightly variable too although at least three samples were taken ateach site Thirty-three samples were collected from eight quarries in Sorbasand 60 quadrats sampled in six quarries in Venta de los Yesos In additiontwenty quadrats from the unaltered scrubland were sampled near the aban-doned quarries (ten per locality) In order to avoid the problem of pseudo-replication each sample was collected far enough from each other Table 3shows complementary methodological details

Data analysis

In order to analyse the behaviour of the species involved in the plant suc-cession in quarries and to detect groups of taxa that follow the same succes-sional pattern species abundance times successional state matrixes were con-structed and subjected to classification (Cluster Analysis) and ordinationanalyses (Correspondence Analysis) by means of the statistical packagePC-ORD (McCune amp Meffo rd 1997) This procedure also allowed toinvestigate whether the successional trends could lead to the recuperationof species composition and relative abundances recorded in the unalteredscrublands considered here as the potential vegetation

For classification procedures Sorensen Jaccard and Kulczynski coeffi-cients were used to build up the similarity matrix (Po dani 1994) and dif-ferent linking strategies attempted (Nearest Neighbour Farthest Neigh-

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

15Plant succession in abandoned gypsum quarries

Rivas-Go day et al 1956 Braun-Blanq uet amp Bo lo s 1958 Rivas-Go day amp Esteve 1965 Rivas-Go day amp Rivas-Martinez 1967 Rivas-Martinez amp Co sta 1970 Lo idi amp Co sta 1997) More recently someother contributions have focussed on the ecological and physiological as-pects (e g Escudero et al 1997 1999 2000a 2000b Merlo et al 19971998 2000 Dana 2000) and on the importance of gypsum soils in the frameof conservation strategies (Cerrillo et al 2002) since many of their speciesare protected at regional national and international levels (Pinto s amp Ro -driguez-Hiraldo 1994 The Red Book of Go mez-Campo (1987) lists12 gypsophytes in Spain Centaurea pinnata Helianthemum alypoides Li-monium album L aragonensis Narcissus tortifolius Nepeta beltranii San-tolina viscosa Teucrium lepicephalum T libanitis T turredanum Thymuslacaitae and T moroderi Nine of them are also included under some of thethreaten category of the IUCN in the recent Red List of Spanish VascularFlora (VVAA 2000) whereas the local endemisms Centaurea pinnataTeucrium lepicephalum T turredanum and Helianthemum alypoides arepriority species for the European Habitats Directive (Ano nymo us 19921997) which also consider the gypsum outgrops and their communities aspriority areas for conservation

The most valuable territories for the conservation of the Iberian gypsumflora are the southeastern lands in the province of AlmerDaggera (Dana 2000)and among these the outcrops of Sorbas-Los Castanos and Tabernas (Cer-rillo et al 2002) These areas harbour one of the worthiest karsts systemson gypsum soils worldwide (Calafo rra amp Pulido -Bo sch 1997) Al-though Sorbas outcrops are partially protected as Natural Area by the An-dalusian Government they are greatly threatened by the intense extractionof gypsum the area is the first European producer of gypsum mineral which causes a dramatic environmental and landscape impact (Fig 1) Theseactivities destroy the karsts systems and alter the rich and original floraof these habitats endangering the further existence of the gypsophilouscommunities

Given these precedents it was considered a priority to study how thesepractices affect the species composition of the pre-existing vascular plantcommunities and to provide the necessary information for the further de-velopment of restoration plans with an ecological basis To achieve this aimin this work the pattern of primary succession is investigated at specieslevel

Study area

The study area is located in the province of AlmerDaggera (SE of the IberianPeninsula) in the Tabernas-Sorbas intermountain basin (Fig 2) which wasformed by evaporates filling during the Messinian Salinity Crisis It is sub-jected to a Mediterranean Macrobioclimate (Rivas-Martinez 1996) andcharacterised by at least two arid months in summer (Fig 3)

Sampled sites (abandoned quarries) were located in Venta de los Yesos(close to Tabernas) and Sorbas-Los Castanos (Fig 2) In both enclaves gyp-

16 J F Mota et al

Fig 1 Abandoned gypsum quarry in Venta de los Yesos

Fig 2 Location of the study areas

17Plant succession in abandoned gypsum quarries

Fig 3 Ombrothermic diagrams from the climatic stations of ldquoLos Gallardosrdquo and ldquoTa-bernasrdquo

sophilous plant communities are dominated by short scrub species with40 in cover whereas the therophytes are scarce and mainly dwell themicrotopographic basins which are formed by deposits of fine materials(Lazaro 1984) The rest of soil is covered by cryptogams a stratum thatcan cover up to 90 of the soil gypsum crusts Two gypsophilous scrub

18 J F Mota et al

Table 2 General distribution of the gypsophytes and their occurrence at the study sitesSorbas and Venta de los Yesos

Gypsophytes Sorbas-Los Venta de DistributionCastanos los Yesos

Coris hispanica X X LocalFrankenia thymifolia ndash X WideGypsophila struthium s str X X WideHelianthemum alypoides X ndash LocalHelianthemum squamatum X X WideHelianthemum syriacum X X WideLepidium subulatum ndash X WideOnonis tridentata X ndash WideSantolina viscosa X X LocalSedum gypsicola X X WideTeucrium turredanum X ndash Local

communities dwell the outcrops Santolino viscosae-Gypsophiletumstruthi i Rivas-Goday amp Esteve 1965 in Venta de los Yesos and Helian-themo alypoidis-Gypsophiletum struthi i (Rivas-Go day amp Esteve1965) Alcaraz et al 1989 in Sorbas both of them belonging to the OrderGypsophil etal ia Bellot amp Rivas Goday in Rivas Goday et al 1997 Thefloristic composition of the two localities is shown in Table 2

Methods

Sampling methods

To approach the problem of the study of successional patterns it was em-ployed the theoretical concept of chronosequence i e the use of differentsuccession states which chronologically ordered give us a sequence of thedynamic of the species and plant communities in a defined interval of timeTwo sets (one per locality Tabernas and Sorbas) of quarries abandoned atdifferent moments in the last 50 years were employed Three successionalstages were consideredStage I (initial) which includes quarries that were abandoned 8ndash 12 yearsagoStage II (or medium) which includes quarries that were abandoned 20ndash 30years agoStage III (or advanced succession) which includes quarries that were aban-doned between 35ndash 70 years ago

We have also considered the scrubland non-disturbed by the quarryingin order to use it as an ecological station of reference or as the potentialnatural vegetation (White amp Walker 1997) Table 2 shows the gypso-phytes of this stadium in each site and their distribution

It must be indicated that the intervals are not continuous since theybelong to different waves of quarries opening by private companies

19Plant succession in abandoned gypsum quarries

Table 3 Study site characteristics location abbreviation time since last intervention sam-pling intensity VY (Venta de los Yesos) SO (Sorbas) FI (stage I abandoned 8ndash 12 yearsago) FII (stage II abandoned 20ndash 30 years ago) FIII (stage III abandoned up to 35 yearsago) M (unaltered shrubland or ldquomatorralrdquo)

Localities Sites UTM Abbreviation Years since last Number ofhuman intervention samplings

(aprox)

Venta de los Los YesosWG30S6204 VYFIndash VYFII 10 20 40 10

YesosWG30S6304 VYM Unknown 10

Cerrillo Blanco WG30S6203 VYFIII 35 10

Penon DDaggeraz WG30S8004 SOFI 10 5

HuelDagger WG30S8003 SOFI 8 5

Los Molinos WG30S8105 SOM Unknown 5

WG30S8309 SOM Unknown 5

Cerron WG30S8310 SOFIIndash SOFIII 25 40 5 3WG30S8409 SOFIIndash SOFIII 25 40 5 3WG30S8410 SOFIIndash SOFIII 25 40 5 2

Sorbas-Los Castanos

Species presence and coverage values were recorded at random in 5 m times5 m quadrats Due to small variations in quarries size the number of sam-ples was slightly variable too although at least three samples were taken ateach site Thirty-three samples were collected from eight quarries in Sorbasand 60 quadrats sampled in six quarries in Venta de los Yesos In additiontwenty quadrats from the unaltered scrubland were sampled near the aban-doned quarries (ten per locality) In order to avoid the problem of pseudo-replication each sample was collected far enough from each other Table 3shows complementary methodological details

Data analysis

In order to analyse the behaviour of the species involved in the plant suc-cession in quarries and to detect groups of taxa that follow the same succes-sional pattern species abundance times successional state matrixes were con-structed and subjected to classification (Cluster Analysis) and ordinationanalyses (Correspondence Analysis) by means of the statistical packagePC-ORD (McCune amp Meffo rd 1997) This procedure also allowed toinvestigate whether the successional trends could lead to the recuperationof species composition and relative abundances recorded in the unalteredscrublands considered here as the potential vegetation

For classification procedures Sorensen Jaccard and Kulczynski coeffi-cients were used to build up the similarity matrix (Po dani 1994) and dif-ferent linking strategies attempted (Nearest Neighbour Farthest Neigh-

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

16 J F Mota et al

Fig 1 Abandoned gypsum quarry in Venta de los Yesos

Fig 2 Location of the study areas

17Plant succession in abandoned gypsum quarries

Fig 3 Ombrothermic diagrams from the climatic stations of ldquoLos Gallardosrdquo and ldquoTa-bernasrdquo

sophilous plant communities are dominated by short scrub species with40 in cover whereas the therophytes are scarce and mainly dwell themicrotopographic basins which are formed by deposits of fine materials(Lazaro 1984) The rest of soil is covered by cryptogams a stratum thatcan cover up to 90 of the soil gypsum crusts Two gypsophilous scrub

18 J F Mota et al

Table 2 General distribution of the gypsophytes and their occurrence at the study sitesSorbas and Venta de los Yesos

Gypsophytes Sorbas-Los Venta de DistributionCastanos los Yesos

Coris hispanica X X LocalFrankenia thymifolia ndash X WideGypsophila struthium s str X X WideHelianthemum alypoides X ndash LocalHelianthemum squamatum X X WideHelianthemum syriacum X X WideLepidium subulatum ndash X WideOnonis tridentata X ndash WideSantolina viscosa X X LocalSedum gypsicola X X WideTeucrium turredanum X ndash Local

communities dwell the outcrops Santolino viscosae-Gypsophiletumstruthi i Rivas-Goday amp Esteve 1965 in Venta de los Yesos and Helian-themo alypoidis-Gypsophiletum struthi i (Rivas-Go day amp Esteve1965) Alcaraz et al 1989 in Sorbas both of them belonging to the OrderGypsophil etal ia Bellot amp Rivas Goday in Rivas Goday et al 1997 Thefloristic composition of the two localities is shown in Table 2

Methods

Sampling methods

To approach the problem of the study of successional patterns it was em-ployed the theoretical concept of chronosequence i e the use of differentsuccession states which chronologically ordered give us a sequence of thedynamic of the species and plant communities in a defined interval of timeTwo sets (one per locality Tabernas and Sorbas) of quarries abandoned atdifferent moments in the last 50 years were employed Three successionalstages were consideredStage I (initial) which includes quarries that were abandoned 8ndash 12 yearsagoStage II (or medium) which includes quarries that were abandoned 20ndash 30years agoStage III (or advanced succession) which includes quarries that were aban-doned between 35ndash 70 years ago

We have also considered the scrubland non-disturbed by the quarryingin order to use it as an ecological station of reference or as the potentialnatural vegetation (White amp Walker 1997) Table 2 shows the gypso-phytes of this stadium in each site and their distribution

It must be indicated that the intervals are not continuous since theybelong to different waves of quarries opening by private companies

19Plant succession in abandoned gypsum quarries

Table 3 Study site characteristics location abbreviation time since last intervention sam-pling intensity VY (Venta de los Yesos) SO (Sorbas) FI (stage I abandoned 8ndash 12 yearsago) FII (stage II abandoned 20ndash 30 years ago) FIII (stage III abandoned up to 35 yearsago) M (unaltered shrubland or ldquomatorralrdquo)

Localities Sites UTM Abbreviation Years since last Number ofhuman intervention samplings

(aprox)

Venta de los Los YesosWG30S6204 VYFIndash VYFII 10 20 40 10

YesosWG30S6304 VYM Unknown 10

Cerrillo Blanco WG30S6203 VYFIII 35 10

Penon DDaggeraz WG30S8004 SOFI 10 5

HuelDagger WG30S8003 SOFI 8 5

Los Molinos WG30S8105 SOM Unknown 5

WG30S8309 SOM Unknown 5

Cerron WG30S8310 SOFIIndash SOFIII 25 40 5 3WG30S8409 SOFIIndash SOFIII 25 40 5 3WG30S8410 SOFIIndash SOFIII 25 40 5 2

Sorbas-Los Castanos

Species presence and coverage values were recorded at random in 5 m times5 m quadrats Due to small variations in quarries size the number of sam-ples was slightly variable too although at least three samples were taken ateach site Thirty-three samples were collected from eight quarries in Sorbasand 60 quadrats sampled in six quarries in Venta de los Yesos In additiontwenty quadrats from the unaltered scrubland were sampled near the aban-doned quarries (ten per locality) In order to avoid the problem of pseudo-replication each sample was collected far enough from each other Table 3shows complementary methodological details

Data analysis

In order to analyse the behaviour of the species involved in the plant suc-cession in quarries and to detect groups of taxa that follow the same succes-sional pattern species abundance times successional state matrixes were con-structed and subjected to classification (Cluster Analysis) and ordinationanalyses (Correspondence Analysis) by means of the statistical packagePC-ORD (McCune amp Meffo rd 1997) This procedure also allowed toinvestigate whether the successional trends could lead to the recuperationof species composition and relative abundances recorded in the unalteredscrublands considered here as the potential vegetation

For classification procedures Sorensen Jaccard and Kulczynski coeffi-cients were used to build up the similarity matrix (Po dani 1994) and dif-ferent linking strategies attempted (Nearest Neighbour Farthest Neigh-

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

17Plant succession in abandoned gypsum quarries

Fig 3 Ombrothermic diagrams from the climatic stations of ldquoLos Gallardosrdquo and ldquoTa-bernasrdquo

sophilous plant communities are dominated by short scrub species with40 in cover whereas the therophytes are scarce and mainly dwell themicrotopographic basins which are formed by deposits of fine materials(Lazaro 1984) The rest of soil is covered by cryptogams a stratum thatcan cover up to 90 of the soil gypsum crusts Two gypsophilous scrub

18 J F Mota et al

Table 2 General distribution of the gypsophytes and their occurrence at the study sitesSorbas and Venta de los Yesos

Gypsophytes Sorbas-Los Venta de DistributionCastanos los Yesos

Coris hispanica X X LocalFrankenia thymifolia ndash X WideGypsophila struthium s str X X WideHelianthemum alypoides X ndash LocalHelianthemum squamatum X X WideHelianthemum syriacum X X WideLepidium subulatum ndash X WideOnonis tridentata X ndash WideSantolina viscosa X X LocalSedum gypsicola X X WideTeucrium turredanum X ndash Local

communities dwell the outcrops Santolino viscosae-Gypsophiletumstruthi i Rivas-Goday amp Esteve 1965 in Venta de los Yesos and Helian-themo alypoidis-Gypsophiletum struthi i (Rivas-Go day amp Esteve1965) Alcaraz et al 1989 in Sorbas both of them belonging to the OrderGypsophil etal ia Bellot amp Rivas Goday in Rivas Goday et al 1997 Thefloristic composition of the two localities is shown in Table 2

Methods

Sampling methods

To approach the problem of the study of successional patterns it was em-ployed the theoretical concept of chronosequence i e the use of differentsuccession states which chronologically ordered give us a sequence of thedynamic of the species and plant communities in a defined interval of timeTwo sets (one per locality Tabernas and Sorbas) of quarries abandoned atdifferent moments in the last 50 years were employed Three successionalstages were consideredStage I (initial) which includes quarries that were abandoned 8ndash 12 yearsagoStage II (or medium) which includes quarries that were abandoned 20ndash 30years agoStage III (or advanced succession) which includes quarries that were aban-doned between 35ndash 70 years ago

We have also considered the scrubland non-disturbed by the quarryingin order to use it as an ecological station of reference or as the potentialnatural vegetation (White amp Walker 1997) Table 2 shows the gypso-phytes of this stadium in each site and their distribution

It must be indicated that the intervals are not continuous since theybelong to different waves of quarries opening by private companies

19Plant succession in abandoned gypsum quarries

Table 3 Study site characteristics location abbreviation time since last intervention sam-pling intensity VY (Venta de los Yesos) SO (Sorbas) FI (stage I abandoned 8ndash 12 yearsago) FII (stage II abandoned 20ndash 30 years ago) FIII (stage III abandoned up to 35 yearsago) M (unaltered shrubland or ldquomatorralrdquo)

Localities Sites UTM Abbreviation Years since last Number ofhuman intervention samplings

(aprox)

Venta de los Los YesosWG30S6204 VYFIndash VYFII 10 20 40 10

YesosWG30S6304 VYM Unknown 10

Cerrillo Blanco WG30S6203 VYFIII 35 10

Penon DDaggeraz WG30S8004 SOFI 10 5

HuelDagger WG30S8003 SOFI 8 5

Los Molinos WG30S8105 SOM Unknown 5

WG30S8309 SOM Unknown 5

Cerron WG30S8310 SOFIIndash SOFIII 25 40 5 3WG30S8409 SOFIIndash SOFIII 25 40 5 3WG30S8410 SOFIIndash SOFIII 25 40 5 2

Sorbas-Los Castanos

Species presence and coverage values were recorded at random in 5 m times5 m quadrats Due to small variations in quarries size the number of sam-ples was slightly variable too although at least three samples were taken ateach site Thirty-three samples were collected from eight quarries in Sorbasand 60 quadrats sampled in six quarries in Venta de los Yesos In additiontwenty quadrats from the unaltered scrubland were sampled near the aban-doned quarries (ten per locality) In order to avoid the problem of pseudo-replication each sample was collected far enough from each other Table 3shows complementary methodological details

Data analysis

In order to analyse the behaviour of the species involved in the plant suc-cession in quarries and to detect groups of taxa that follow the same succes-sional pattern species abundance times successional state matrixes were con-structed and subjected to classification (Cluster Analysis) and ordinationanalyses (Correspondence Analysis) by means of the statistical packagePC-ORD (McCune amp Meffo rd 1997) This procedure also allowed toinvestigate whether the successional trends could lead to the recuperationof species composition and relative abundances recorded in the unalteredscrublands considered here as the potential vegetation

For classification procedures Sorensen Jaccard and Kulczynski coeffi-cients were used to build up the similarity matrix (Po dani 1994) and dif-ferent linking strategies attempted (Nearest Neighbour Farthest Neigh-

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

18 J F Mota et al

Table 2 General distribution of the gypsophytes and their occurrence at the study sitesSorbas and Venta de los Yesos

Gypsophytes Sorbas-Los Venta de DistributionCastanos los Yesos

Coris hispanica X X LocalFrankenia thymifolia ndash X WideGypsophila struthium s str X X WideHelianthemum alypoides X ndash LocalHelianthemum squamatum X X WideHelianthemum syriacum X X WideLepidium subulatum ndash X WideOnonis tridentata X ndash WideSantolina viscosa X X LocalSedum gypsicola X X WideTeucrium turredanum X ndash Local

communities dwell the outcrops Santolino viscosae-Gypsophiletumstruthi i Rivas-Goday amp Esteve 1965 in Venta de los Yesos and Helian-themo alypoidis-Gypsophiletum struthi i (Rivas-Go day amp Esteve1965) Alcaraz et al 1989 in Sorbas both of them belonging to the OrderGypsophil etal ia Bellot amp Rivas Goday in Rivas Goday et al 1997 Thefloristic composition of the two localities is shown in Table 2

Methods

Sampling methods

To approach the problem of the study of successional patterns it was em-ployed the theoretical concept of chronosequence i e the use of differentsuccession states which chronologically ordered give us a sequence of thedynamic of the species and plant communities in a defined interval of timeTwo sets (one per locality Tabernas and Sorbas) of quarries abandoned atdifferent moments in the last 50 years were employed Three successionalstages were consideredStage I (initial) which includes quarries that were abandoned 8ndash 12 yearsagoStage II (or medium) which includes quarries that were abandoned 20ndash 30years agoStage III (or advanced succession) which includes quarries that were aban-doned between 35ndash 70 years ago

We have also considered the scrubland non-disturbed by the quarryingin order to use it as an ecological station of reference or as the potentialnatural vegetation (White amp Walker 1997) Table 2 shows the gypso-phytes of this stadium in each site and their distribution

It must be indicated that the intervals are not continuous since theybelong to different waves of quarries opening by private companies

19Plant succession in abandoned gypsum quarries

Table 3 Study site characteristics location abbreviation time since last intervention sam-pling intensity VY (Venta de los Yesos) SO (Sorbas) FI (stage I abandoned 8ndash 12 yearsago) FII (stage II abandoned 20ndash 30 years ago) FIII (stage III abandoned up to 35 yearsago) M (unaltered shrubland or ldquomatorralrdquo)

Localities Sites UTM Abbreviation Years since last Number ofhuman intervention samplings

(aprox)

Venta de los Los YesosWG30S6204 VYFIndash VYFII 10 20 40 10

YesosWG30S6304 VYM Unknown 10

Cerrillo Blanco WG30S6203 VYFIII 35 10

Penon DDaggeraz WG30S8004 SOFI 10 5

HuelDagger WG30S8003 SOFI 8 5

Los Molinos WG30S8105 SOM Unknown 5

WG30S8309 SOM Unknown 5

Cerron WG30S8310 SOFIIndash SOFIII 25 40 5 3WG30S8409 SOFIIndash SOFIII 25 40 5 3WG30S8410 SOFIIndash SOFIII 25 40 5 2

Sorbas-Los Castanos

Species presence and coverage values were recorded at random in 5 m times5 m quadrats Due to small variations in quarries size the number of sam-ples was slightly variable too although at least three samples were taken ateach site Thirty-three samples were collected from eight quarries in Sorbasand 60 quadrats sampled in six quarries in Venta de los Yesos In additiontwenty quadrats from the unaltered scrubland were sampled near the aban-doned quarries (ten per locality) In order to avoid the problem of pseudo-replication each sample was collected far enough from each other Table 3shows complementary methodological details

Data analysis

In order to analyse the behaviour of the species involved in the plant suc-cession in quarries and to detect groups of taxa that follow the same succes-sional pattern species abundance times successional state matrixes were con-structed and subjected to classification (Cluster Analysis) and ordinationanalyses (Correspondence Analysis) by means of the statistical packagePC-ORD (McCune amp Meffo rd 1997) This procedure also allowed toinvestigate whether the successional trends could lead to the recuperationof species composition and relative abundances recorded in the unalteredscrublands considered here as the potential vegetation

For classification procedures Sorensen Jaccard and Kulczynski coeffi-cients were used to build up the similarity matrix (Po dani 1994) and dif-ferent linking strategies attempted (Nearest Neighbour Farthest Neigh-

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

19Plant succession in abandoned gypsum quarries

Table 3 Study site characteristics location abbreviation time since last intervention sam-pling intensity VY (Venta de los Yesos) SO (Sorbas) FI (stage I abandoned 8ndash 12 yearsago) FII (stage II abandoned 20ndash 30 years ago) FIII (stage III abandoned up to 35 yearsago) M (unaltered shrubland or ldquomatorralrdquo)

Localities Sites UTM Abbreviation Years since last Number ofhuman intervention samplings

(aprox)

Venta de los Los YesosWG30S6204 VYFIndash VYFII 10 20 40 10

YesosWG30S6304 VYM Unknown 10

Cerrillo Blanco WG30S6203 VYFIII 35 10

Penon DDaggeraz WG30S8004 SOFI 10 5

HuelDagger WG30S8003 SOFI 8 5

Los Molinos WG30S8105 SOM Unknown 5

WG30S8309 SOM Unknown 5

Cerron WG30S8310 SOFIIndash SOFIII 25 40 5 3WG30S8409 SOFIIndash SOFIII 25 40 5 3WG30S8410 SOFIIndash SOFIII 25 40 5 2

Sorbas-Los Castanos

Species presence and coverage values were recorded at random in 5 m times5 m quadrats Due to small variations in quarries size the number of sam-ples was slightly variable too although at least three samples were taken ateach site Thirty-three samples were collected from eight quarries in Sorbasand 60 quadrats sampled in six quarries in Venta de los Yesos In additiontwenty quadrats from the unaltered scrubland were sampled near the aban-doned quarries (ten per locality) In order to avoid the problem of pseudo-replication each sample was collected far enough from each other Table 3shows complementary methodological details

Data analysis

In order to analyse the behaviour of the species involved in the plant suc-cession in quarries and to detect groups of taxa that follow the same succes-sional pattern species abundance times successional state matrixes were con-structed and subjected to classification (Cluster Analysis) and ordinationanalyses (Correspondence Analysis) by means of the statistical packagePC-ORD (McCune amp Meffo rd 1997) This procedure also allowed toinvestigate whether the successional trends could lead to the recuperationof species composition and relative abundances recorded in the unalteredscrublands considered here as the potential vegetation

For classification procedures Sorensen Jaccard and Kulczynski coeffi-cients were used to build up the similarity matrix (Po dani 1994) and dif-ferent linking strategies attempted (Nearest Neighbour Farthest Neigh-

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

20 J F Mota et al

bour UPGMA and Wardrsquos Method) in order to test for the constancy ofthe groups the robustness of the results obtained (Legendre amp Legendre1999) Since the results found were very similar only those obtained usingWardrsquos Method are shown Correspondence Analysis was employed to de-scribe the theoretical relationships of dependence between sets of characters(Gauch 1982 Hair et al 1999 McGarical et al 2000)

Finally we have built frequency histograms which show the relativeabundance of the mentioned groups in every successional stage establishedIt must be noted that in order to extract meaningful information about theplant succession as related to the ecological preference by gypsum soilthe species recorded were classified as gypsophytes or non-gypsophytesaccording to the previous proposals (Rivas-Martinez amp Co sta 1970Lo idi amp Co sta 1997 Lazaro 1986 Merlo et al 1998 2000) Gypsophilastruthium subsp struthium is an obligated gypsophyte endemic in the Ibe-rian Peninsula which shows higher cover in the first successional stage inrelation to other gypsophytes (Merlo et al 1997) so we have treated thistaxon as an independent group

Results

Cluster analyses made for the samples taken in Sorbas (Fig 4a) showedtwo groups of species with different behaviour along the successional se-quence The first group harboured mainly gypsophytes (such as Helian-themum squamatum Santolina viscosa Teucrium turredanum Coris his-panica and Ononis tridentata) and some non-gypsophytes appearing inthe unaltered scrublands (Elaeoselinum tenuifolium Helianthemum syr-iacum and Launaea lanifera) The second group was mainly formed byruderal taxa characteristic of disturbed habitats (such as Andryala ragus-ina Artemisia barrelieri Dittrichia viscosa Eryngium campestre Piptath-erum miliaceum) The analyses also included into this group the obligategypsophyte Gypsophila struthium subsp struthium which shows highercoverage values in the first states of the successional sequence than in thenon-altered scrubland together with the local endemism Helianthemumalypoides recorded in the stage II of the succession (20ndash 25 years of work-out)

This pattern matched that of Venta de los Yesos (Fig 4b) Cluster analy-ses grouped the gypsophytes Coris hispanica Frankenia thymifolia Santol-ina viscosa and Helianthemum squamatum together with non-obligate gyp-sophytes such as Helianthemum syriacum The second group was formedmainly by non-gypsophytes ndash mainly ruderals ndash with a great colonisationpower (Andryala ragusina Artemisia glutinosa Diplotaxis lagascana) Asin the case of Sorbas Gypsophila struthium subsp struthium and Lepidiumsubulatum ndash other obligated gypsophyte ndash appeared again in the assem-blage of ruderals and non-gypsophytes

These patterns were also supported by frequency histograms Fig 5a andc shows the special behaviour of Gypsophila struthium subsp struthium as

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

21Plant succession in abandoned gypsum quarries

a

b

Fig 4 Cluster analysis of the floristic data samples in Sorbas (a) and Venta de los Yesos(b) using Wardrsquos method Similarity has been obtained by means of Sorensen coefficientusing the species cover in the plots Obligated gypsophytes are shown in boldface Forspecies names see Tab 1

compared to the other gypsophytes it is the dominant species in the earliestsuccessional states in both localities (Venta de los Yesos and Sorbas-LosCastanos) and its coverage decreases as the succession advances reachingthe lowest abundance in the non-altered scrubland The case of the remain-ing gypsophytes is the opposite They reach the greatest abundance valuesin the latest stages (stages III and IV) From the chorological point of viewlocal endemism entered in the latest succesional stages (Fig 5b and d) whilebroadly distributed taxa (such as Gypsophila struthium subsp struthium orLepidium subulatum entered in the first years of the sequence

Correspondence Analysis showed that 75 of the data variance couldbe explained by means of two axes (Fig 6a and b) Axis 1 separated thesamples taken in the non-altered scrubland from those taken in the quarriesAxis 2 ordered the samples taken in each quarry showing a successionalpattern from stage I to stage III and left aside the releves taken in themature stands

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

22 J F Mota et al

a

b

c

dFig 5 Frequency histograms of the species groups established in different successionalstages a + b Sorbas c + d Venta de los Yesos Abbreviations gypsophytes (Obl gyp)non-gypsophytes (Non-gyp) Gypsophila struthium (Gyp_str) local gypsophytes (Locgyp) gypsophytes with wider distribution (Wid gyp) For further abbreviations used inthe diagrams see Table 3

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

23Plant succession in abandoned gypsum quarries

Fig 6a

Table 4 Cover percentage of the gypsophytes in Sorbas and in Venta de los Yesos

Species Sorbas Venta de los Yesos

Coris hispanica 075 107Frankenia thymifolia ndash 275Gypsophila struthium s str 475 176Helianthemum alypoides 012 ndashHelianthemum squamatum 105 28Launaea fragilis 026 077Lepidium subulatum ndash 135Santolina viscosa 205 361Teucrium turredanum 121 ndash

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

24 J F Mota et al

b

Fig 6 Correspondence Analysis (CA) for the samples collected in Sorbas (a) and Ventade los Yesos (b) in each successional stage For abbreviations see Table 3 Each sample isshown using Pn where ldquonrdquo is the number of the sample taken in each stage

Discussion and conclusions

From the floristic point of view the primary succession in gypsum soils ofthe southeast of Spain can be defined as an auto-succession or direct succes-sion (Shreve 1942) as the dominant species that take part in the dynamicprocesses are those appearing in the undisturbed communities This patterncan be attributable to the peculiar characteristics of gypsum soils and to theexistence of a pool of gypsophytes which are well adapted to dwell onthese soils After quarries work-out the most important pioneer is Gyp-sophila struthium subsp struthium which is the most abundant throughoutthe initial stages of succession (i e first 25 years) This suggests that thespecies shows a marked preference for disturbed gypsum soils and that it

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

25Plant succession in abandoned gypsum quarries

profits from human impact in these environments Gypsophila struthiumsubsp struthium and to a lesser extent also Lepidium subulatum ndash both ofthem widely distributed taxa ndash are the only gypsophytes showing markedcolonising abilities after disturbance The finding is specially surprising ifwe take into account that the ecological behaviour of the remaining gypso-phytes and more particularly that of narrowly distributed species is justthe opposite as they enter in the abandoned soils only in the latest momentof the successional catena

Although it is not possible to give a definitive reason for this peculiarecological behaviour a subject which merits further monographic studiesit can be thought that Gypsophila struthium subsp struthium shares one ormore of the traits with specialists colonising recently opened sites (such asAndryala ragusina or Dittrichia viscosa) while it is also assisted with oneor more of the autecological traits of the remaining gypsophytes that atleast allow this species to persist in the non-disturbed soils Thereforealthough nowadays there are few studies dealing with this recent observa-tion (Van der Valk 1992) first attention should be paid to those auteco-logical traits of primo-colonisers (high growth rates greater dispersion abil-ities rapid germination high seed and seedling production greater toler-ance to nutrient-poor soils etc)

A quick inspection of Gypsophila propagules shows that they are notequipped with any obvious dispersal mechanism and that their size doesnot greatly differ to that of the remaining gypsophytes It has been ob-served that survival rates of Gypsophila seedlings can be slightly greaterthan the remaining gypsophytes and that the species germinates rapidly(Merlo et al 1997 Dana 2000) while some authors have proposed thatin long-term development these small differences could play a role in com-munities composition (Llo ret 1998) However more investigation aboutthese and other traits of the gypsophytes aforementioned are required be-fore making any conclusive remark

Finally at a first sight there is not a clear relationship between the distri-butional amplitude of the gypsophytes and their corresponding colonisa-tion ability The colonists Gypsophila struthium subsp struthium and Lepi-dium subulatum are widely distributed whereas amongst the late succes-sional stages species with both narrow (Helianthemum alypoides andTeucrium turredanum) and broad (Helianthemun squamatum Ononis tri-dentata) distributions can be found However it cannot be easily answeredif this fact is a coincidence or the result of biogeographical andor ecologicalprocesses It is clear however that all the local endemism such as Helian-themum alypoides and Teucrium turredanum are poor colonisers and thatthis should be taken into consideration in the planning of the human-activi-ties on gypsum soils (Cerrillo et al 2001 Cueto et al 1999)

Moreover it must be highlighted that in terms of presence of the speciesthe recuperation was relatively fast while this was not so for the relativeabundances In a preliminary work studying how the quarring affects theecological groups of gypsophytes cryptograms and therophytes we arrivedat this conclusion (Mota et al 1999) This shows the difficulties for the

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

26 J F Mota et al

rare and endangered gypsophilous species in recovering their demographi-cal levels after such a strong disturbance and remarks on the necessity ofimplementing a more rational economical exploitation of the gypsum de-posits under semiarid climate According to the general view of the islandtheory (Shafer 1990 Whittaker 1998) the consequences of the reductionand fragmentation of the habitats of the gypsophytes could lead to anincrease in the probability of extinction at local and regional level of someof the studied species

Acknowledgements Sincere thanks are due to Prof Ulrich Deil and to one anonymousreferee for their suggestions which notably improved the quality of earlier drafts Thisresearch was financially supported by two grants from the DGES (PB95ndash 0959 andPB98ndash 1385) and from the CompanDaggera Minera Fuente del Peral We deeply acknowledgethe help provided by R S McMichael and by Ma A Munoz with the English language

References

Anonymous (1992) Directive 9243 of the Council of the European Community onthe Conservation of Habitats and Wild Fauna and Flora ndash European CommunityBrussels

ndash (1997) Directive 9762 of the Council of the European Community on the Conserva-tion of Habitats and Wild Fauna and Flora ndash European Community Brussels

Braun-Blanquet J amp Bolos O (1958) Les groupements vegetaux du bassin moyen delrsquoEbre et leur dynamisme ndash An Estac Exp Aula Dei 5 1ndash 4 [1957]

Calaforra J M amp Pulido-Bosch A (1997) Peculiar landforms in the gypsum karst ofSorbas (Southeastern Spain) ndash Carbonates and evaporites 12(1) 110ndash 116

Campbell R S amp Campbell I F (1938) Vegetation on gypsum soils of the Jordana PlainNew Mexico ndash Ecology 19 572ndash 577

Castroviejo S et al (eds) (1990 1993 1997 1999) Flora Iberica Vol 2 4 5 y 7 ndashC S IC Madrid

Cerrillo M I Mota J F Perez GarcDaggera F J Castro H amp Dana E (2001) Datos para laconservacion de Helianthemum alypoides Losa amp Rivas-Goday ndash In Cano CarmonaE GarcDaggera Fuentes A Torres Cordero J A amp Salazar MendDaggeras C (eds) Valoracion yGestion de Espacios Naturales pp 105ndash 112 ndash Universidad de Jaen Espana

Cerrillo M I Dana E D Castro H RodrDaggerguez-Tamayo M L amp Mota Poveda J F(2002) Seleccion de areas prioritarias para la conservacion de flora gipsDaggercola en elsureste de la PenDaggerncula Iberica ndash Rev Chil Hist Nat 75(2) 395ndash 408

Cueto Romero M Fernandez Jurado M A Lopez Cerrillo M I Marquez PayesJ M Munoz Gonzalez C Perez GarcDaggera F J RodrDaggerguez Tamayo M L SanchezManas M Serrano Munoz M M Sola Gomez A J amp Mota Poveda J F (1999) Larestauracion de las canteras de yesos iquestQue flora se debe utilizar ndash In NavarroFlores A Sanchez Garrido J A amp Collado Fernandez D M (eds) MinerDaggera Indu-stria y Medio Ambiente en la Cuenca Mediterranea pp 69ndash 80 ndash Universidad deAlmerDaggera Espana

Dana E (2000) Estudio de la Sucesion Vegetal en canteras de yeso abandonadas y suaplicacion a la conservacion de la Flora y Vegetacion de los Aljezares Ibericos ndash TesisDoctoral Universidad de AlmerDaggera 274 pp

Duvigneaud P amp Denaeyer-De Smet S (1966) Accumulation du soufre dans quelquesespeces gypsophiles drsquoEspagne ndash Bull Soc Bot Belg 99 263ndash 269

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

27Plant succession in abandoned gypsum quarries

ndash (1968) Essai de classification chemique (elements mineraux) de plantes gypsicoles duBassin lrsquoEbre ndash Bull Soc R Bot Belg 101 279ndash 291

Emerson F W (1935) An ecological reconnaissance in the White Sands New Mexico ndashEcology 16 226ndash 233

Escudero A Carnes L F amp Perez-Garc Daggera F (1997) Seed germination of gypsophitesand gypsovags in semi-arid central Spain ndash J Arid Environ 36 487ndash 497

Escudero A Somolinos R C Olano J M amp Rubio A (1999) Factors controllingthe establishment of Helianthemum squamatum an endemic gypsophile of Semi-AridSpain ndash J Ecol 87 290ndash 302

Escudero A Albert M J Pita J M amp Perez-Garc Daggera F (2000a) Inhibitory effects ofArtemisia herba-alba on the germination of the gypsophyte Helianthemum squama-tum ndash Plant Ecol 148 71ndash 80

Escudero A Iriondo J M Olano J M Rubio A amp Somolinos R C (2000b) Factorsaffecting the establishment of a gypsophite The case of Lepidium subulatum (Brassica-ceae) ndash Am J Bot 87(6) 861ndash 871

Gauch H C (1982) Multivariate analysis in Community Ecology ndash Cambridge Univer-sity Press Cambridge 298 pp

Gomez-Campo C (ed) (1987) Libro Rojo de Especies Vegetales Amenazadas de EspanaPeninsular y Baleares ndash ICONA Madrid 678 pp

Hair J F Anderson R E Tatham R L amp Black W C (1999) Analisis Multivariante5a Ed ndash Prentice Hall Iberia Madrid 799 pp

Johnston I M (1941) Gypsophily among Mexican Desert Plants ndash J Arnold Arbor22 145ndash 170

Lazaro R (1984) Contribucion al estudio de la flora y vegetacion gipsDaggercola de la provin-cia de AlmerDaggera ndash Tesis de Licenciatura Universidad de Malaga 296 pp

ndash (1986) Sobre la flora y vegetacion gipsDaggercola almeriense (Fanerogamas) ndash Bol InstEstud Almer 6 131ndash 150

Legendre P amp Legendre L (1999) Numerical Ecology Developments in environmentalmodelling 20 ndash Elsevier Amsterdam 853 pp

Lloret F (1998) Fire canopy and seedling dynamics in Mediterranean shrubland ofnortheastern Spain ndash J Veg Sci 9 417ndash 430

Loidi J amp Costa M (1997) SintaxonomDaggera de los matorrales gipsDaggercolas espanoles ndashFitosociologia 32 221ndash 227

Lopez Gonzalez G (1980) Launaea fragilis Asso Pau nombre correcto para L resedi-folia auct plur nom (L) Kuntze ndash An Jard Bot Madr 36 135ndash 138

McCune B amp Mefford M J (1997) PC-ORD Multivariate Analysis of Ecological dataVersion 30 MjM Software Design ndash Gleneden Beach Oregon Usa 47 pp

McGarical K Cushman S amp Stanfford S (2000) Multivariate Statistic for Wildlife andEcology Research ndash Springer-Verlag NY 283 pp

Merlo M E Cabello J Marquez M M amp Aleman M M (1997) On the germinationof plants on gypseous soils in relation to the medium calcium content ndash 36th IAVSSymposium Island and high mountain vegetation Biodiversity Bioclimate and Con-servation Proceeding Book ndash Serie Informes 40 197ndash 206

Merlo M E Mota J F Cabello J amp Aleman M M (1998) La gipsofilia en plantasun apasionante edafismo ndash Investig Gest Medio Nat 3 103ndash 112

Merlo M E RodrDaggerguez-Tamayo M L Jimenez M L amp Mota J F (2000) Recapitu-lacion sobre el comportamiento biogeoquDaggermico de algunos gipsofitos y halofitos iber-icos ndash Monogr Flora Veg betica 12 97ndash 106

Meyer S (1986) The ecology of gypsophile endemism in the Eastern Mojave Desert ndashEcology 67 1303 ndash 1313

28 J F Mota et al

Mota Poveda J F Merlo E Oyonarte C Penas J Perez-Garc Daggera F J RodrDaggerguez-Tamayo M L Aguilera A Bonilla G Cabello J Cueto M Dana E FernandezJurado M A Sola Gomez A J amp Lopez-Cerrillo M (1999) Canteras de yeso Suce-sion Vegetal y Planes de Restauracion ndash In Navarro A Sanchez J A amp ColladoD M (eds) MinerDaggera Industria y Medio Ambiente en la Cuenca Mediterraneapp 83ndash 93 ndash Universidad de AlmerDaggera Espana

Parsons P F (1976) Gypsophily in plants ndash a review ndash Am Midl Nat 96 1ndash 20Pintos M R amp RodrDaggerguez-Hiraldo C (1994) Desarrollo Legislativo a nivel internacio-

nal nacional y autonomico ndash In Hernandez-Bermejo E amp Clemente M (eds)Proteccion de la flora de AndalucDaggera pp 195ndash 208 ndash ConsejerDaggera de Medio AmbienteJunta de AndalucDaggera Sevilla

Podani J (1994) Multivariate Analysis in Ecology and Systematics A methodogicalguide to the SYN-TAX 50 Package ndash Ecological Computations Series (ECS) vol 6SPB Academic Publishing bv The Hague The Netherlands 316 pp

Powell A M amp Turner B L (1977) Aspects of the plant biology of the gypsumoutcrops of the Chihuahuan Desert ndash U S National Park Service Trans ProcSeries 3 315ndash 325

Rivas Goday S amp Rivas-Mart Daggernez S (1967) Matorrales y tomillares de la PenDaggernsulaIberica comprendidos en la Clase Ononido-Rosmarinetea Br-Bl 1947 ndash An InstBot A J Cavanilles 25 5ndash 201

Rivas Goday S amp Steve F (1965) Nuevas comunidades de tomillares del sureste aridoiberico ndash An Inst Bot A J Cavanilles 23 7ndash 78

Rivas Goday S Borja Carbonell J Monasterio Fernandez A Fernandez Galiano ERigual Magallon A amp Rivas MartDaggernez S (1956) Aportaciones a la FitosociologDaggeraHispanica Proyectos De Comunidades Hispanicas II ndash An Inst Bot A J Cavanil-les 14 435ndash 500

Rivas MartDaggernez S (1996) Geobotanica y bioclimatologDaggera ndash Discurso del Acto de Investi-dura de Doctor Honoris Causa Serv Publ Univ Granada 98 pp

Rivas MartDaggernez S amp Costa M (1970) Comunidades gipsDaggercolas del centro de Espana ndashAn Inst Bot A J Cavanilles 27 193ndash 224

Shafer C L (1990) Nature Reserves ndash Smithsonian Institution Press Washington189 pp

Shreve F (1942) The desert vegetation of North America ndash Bot Rev 8 195ndash 246Tutin T G Heywood V H Burges N A Moore D M Valentine D H Walters

S M amp Webb D A (eds) (1964 ndash 1980) Flora Europaea Vol 1ndash 5 ndash Cambridge UnivPress Cambridge

Van der Valk A G (1992) Establishment colonization and persistence ndash In Glenn-Levin D C Peet R K amp Veblen T T (eds) Plant Succession theory and predic-tion pp 60ndash 102 ndash Chapman amp Hall London

VVAA (2000) Lista Roja de Flora Vascular Espanola ndash Conserv Veg 6 (extra) 11ndash 38Watson A (1979) Gypsum crusts in deserts ndash J Arid Environ 2 3ndash 20White P S amp Walker J L (1997) Aproximating naturersquos variation selecting and using

reference information in restoration ecology ndash Restor Ecol 5 338ndash 349Whittaker R H (1998) Island Biogeography ndash Oxford University Press Oxford 285 pp

Addresses of the authorsJuan Francisco Mota Ana Jose So la ElDaggeras David Dana amp MarDaggera Luisa Jim enez-Sanchez Departamento de BiologDaggera Vegetal y EcologDaggera Facultad de Ciencias Experimen-tales Universidad de AlmerDaggera Carretera Sacramento La Canada de San Urbano sn04120 AlmerDaggera Spain Fax +3 49 50 01 50 69 Author for correspondence e-mail jmotauales