SOFT-WATER VEGETATION (LITTORELLION) IN SPANISH MOUNTAINS
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1 Folia Geobotanica 34: , 1999 SOFT-WATER VEGETATION (LITTORELLION) IN SPANISH MOUNTAINS Jose A. Molinal), Santiago Sardinero 2 ) & Concepcion Pertinez l ) 1) Departamento de Biologia Vegetall/, Universidad Complutense de Madrid, E-284 Madrid, Spain; fax , jmabril@eucmax.sim.ucm.es 2) Instituto Nacional de Investigaciones Agrarias, Centra de Investigaci6n Forestal, E-284 Madrid, Spain; sardiner@inia.es Keywords: Aquatic vegetation, Classification, High mountains, Littorelletea, Ordination, Phytosociology Abstract: This paper presents a systematic review of Spanish high mountain soft water communities based on 46 phytosociological releves. Using a numerical analysis with ordination (correspondence analysis - CA) and classification (Jaccard index and complete-linkage clustering) three groups corresponding to the phytosociological associations Isoeto lacustris-sparganietum borderei, Sparganio angustifolii-isoetetum echinospori and Sparganio angustifolii-callitrichetum font-queri have been defined. Spanish Littorellion communities are characterized by boreal-alpine and endemic elements. The boreal-alpine elements probably spread via the Pyrenees-Iberian System through to the mountains of the western peninsula during a cold period, thus sharing the habitat with the Ibero-Atlantic flora which was able to adapt to the changing climatic conditions. INTRODUCTION The Littorellion alliance characterizes oligotrophic stands of small limnophytes which consist of a small number of species belonging to highly specialized flora. This vegetation is composed of vascular, rooted plants arranged in two layers: the top layer dominated by Sparganium angustifolium and the bottom layer, a submerged sward, frequently dominated by the Isoetes species. The Littorellion alliance is especially widespread in lowland ponds and lakes in northern and western Europe, but also occurs in high mountain ranges in central and southern Europe (PIETSCH 1971, DIERSSEN 1975, OBERDORFER 1977, SCHAMINEE et al. 1992). SCHAMINEE et al. (1995) have noted the occurrence of Sparganium angustifolium communities together with Sphagnum species belonging to the class Scheuchzerietea in moorland ponds in the Netherlands. From a syntaxonomic viewpoint, NAVARRO (1987) identified five associations of limited geographic importance within the Littorellion alliance in the Iberian Peninsula: Isoeto lacustris-sparganietum borderei (Pyrenees), Sparganio angustifolii-isoetetum echinospori (Iberian System), Sparganio angustifolii-callitrichetum font-queri (Cantabrian Mountains), Sparganio angustifolii-isoetetum velati (Sierra de Gredos in the Central System), and Subulario aquaticae-isoetetum asturicensis (Sierra de Bejar in the Central System). This study makes a syntaxonomic review of the Littorellion alliance in Spain and synthesizes the syntaxa that have been described into three associations. Furthermore, it formulates a hypothesis about the origin of the endemic element of the flora which characterizes this alliance in the Iberian Peninsula.
2 254 JA Molina et at. MATERIAL AND METHODS The study is based on a data matrix comprised of 46 releves and 28 species sampled according to the BRAUN-BLANQUET (1979) method. The authors have contributed sixteen original releves from the Spanish Central System and the remaining releves have been taken from literature on these communities in the Spanish high mountains, specifically in the Pyrenees, the Cantabrian Mountains, the Iberian System and the Central System (BRAUN-BLANQUET 1948, RIVAS GODAY & RIVAS-MARTINEZ 1959, RrvAs-MARTINEZ 1963, NAVARRO et a , NAVARRO 1987, CARRILLO & NINOT 1992). Only those releves which include at least the Isoetes species and Sparganium angustifolium have been included in the data matrix. For data classification, the resemblance matrix between releves was calculated using the Jaccard index (presence/absence), which is widely used in biogeographical studies (DUFRENE & LEGENDRE 1991). The releves were grouped by means of complete linkage with the help of the SYN-TAX program (PODANI 1993). For data ordination, the Braun-Blanquet cover values were transformed into a 1-9 scale proposed by VAN DER MAAREL (1979). The data matrix obtained was subjected to correspondence analysis (CA) using the CANOCO program (TER BRAAK 1985). The taxa names of vascular plants are given according to CASTROVIEJO et al. ( ) and TUTIN et a1. ( ), except in the case of Antinoria agrostidea subsp. natans (HAECKEL) RNAS-MART. and Isoetes velatum subsp. velatum f. lereschii (RCHB. f.) PRADA. The terms referring to biotypes are those used by DEN HARTOG & SEGAL (1964). Phytogeographically, the term "Ibero-Atlantic" relates to the western territories of the Iberian Peninsula. RESULTS AND DISCUSSION Classification The dendrogram in Fig. 1 shows three clearly distinguishable groups, with Isoetes species acting as characteristic taxa among the dominant plants (Tab. 1). Group A includes only Pyrenean releves and is characterized by Isoetes lacustre (Tab. 1, releves 1-5). This group is assigned to the Isoeto lacustris-sparganietum borderei association which was described in the eastern Pyrenees, where I. lacustre has its southemmost distribution in Europe (BRAUN-BLANQUET 1948). Group B corresponds to Pyrenean and Iberian System releves characterized by Isoetes echinosporum. All of these releves are assigned to the Sparganio angustifolii-isoetetum echinospori association (Tab. 1, releves 6-24). A shallow water variant has been distinguished growing on the shores of lakes and in semi-silted pools with ]uncus bulbosus as differential taxon (subgroup Bb; Tab. 1, releves 18-24). Sparganio angustifolii-isoetetum echinospori was described in the Iberian System (NAVARRO 1987) where I. echinosporum reaches its southemmost distribution in Spain. Group C (Tab. 1, releves 25-46) includes the communities characterized by Isoetes velatum s. 1. which are assigned here to the Sparganio-Callitrichetum font-queri association found along the western Central System (Sierra de Gredos and Sierra de Bejar) and in the western Cantabrian Mountains.
3 Littorellion in Spain 255 Table I. Littorellion communities in Spain. 1-5 Isoeto lacustris-sparganietum borderei (group A), 6-24 Sparganio angustifolii-isoeteturn echinospori (group B) and Sparganio angustifolii-callitrichetum font-queri (group C). Trinomial names have been abreviated into binomial names in the following cases: Antinoria agrostidea subsp. notans and Sphagnum auriculaturn var. inundatum. The taxon referred here as Isoetes velatum (s.l.) includes only the microtaxa endemic to the western Spain. Group Subgroup No. of column AAAAA BBBBBBBBBBBBBBBBBBB CCCCCCCCCCCCCCCCCCCCCC aaaaaaaaaaaabbbbbbb Characteristics of the Lit/ore/lion Sparganium angustifolium Subularia aquatica Isoetes lacustre Isoetes echinosporum Littorella uniflora Isoetes velatum s.1. Antinoria natans Differentials of the associations Callitriche palustris +... Baldellia alpestris Juncus bulbosus Callitriche brutia Potamogeton natans Ranunculus ololeucos Other taxa Carex rostrata Alopecurus aequalis Drepanocladus exannulatus Equisetum limosum Myriophyllum alterniflorurn Ranunculus aquatilis Potamogeton polygonifolius Ranunculus peltatus Phi/onotis fontana Potamogeton alpinus Glyceria declinata Ranunculus flammula Carex vesicaria Fontinalis antipyretica Sphagnum inundatum Localities: 1 Etang Long, 2 Etang de L1ose, 3 Etang de Balmette, 4 Etang de Balleil (BRAUN-BLANQUEf 1948); 5 Estanys de la L1osa, 6 Estanys de les Mangades, 14 and 15 Estanys de Trescuro (CARRILLO & NINOT 1992); 7 and 2 Laguna Larga de Urbi6n (NAVARRO 1987); 8 and 9 Laguna Negra de Neila (NAVARRO 1987); 1, 11, 12, 16 and 17 Laguna Helada de Urbi6n (NAVARRO 1987); 13, 18,21 and 24 Laguna Larga de Neila (NAVARRO 1987); 19 and 22 Laguna de las Pardillas de Neila (NAVARRO 1987); 23 Laguna Negra de Urbi6n (NAVARRO 1987); 25, 26, 27, 37 and 44 Navalguijo, Laguna de los Caballeros (*); 28, 38 and 39 Navalperal de Tormes, arroyo de las Pozas (*); 29 Solana de Avila, laguna Negra (*); 3, 31, 32 and 33 Solana de Avila, lagunas del Trampal (*); 34 and 45 Solana de Avila, lagunas del Trampal (NAVARRO et al. 1979); 35, 36 and 4 Navalperal de Tormes, Laguna Grande de Gredos (*); 41 and 43 Navalperal de Tormes, Laguna Grande de Gredos (RIVAS-MARTlNEZ 1963); 42 Navalperal de Tormes, arroyo de las Pozas (RIVAs-MARTINEZ 1963); 46 Laguna de Arbas, Leitariegos (RIVAS GoDAY & RIVAS-MARTlNEZ 1959). The releves made by the authors are followed by an asterisk in brackets and those taken from the literature are followed by the bibliographic reference in brackets.
4 256 J.A. Molina et al..9 A I B C.8 r-'- B~ Bb I ( I O.J. Fig. 1. Hierarchical clustering using Jaccard index and complete linkage of 46 Littorellion releves from Spain. Numbers of releves correspond to those in Tab. 1. Ordination CA ordination separates the three groups identified in the classification analysis quite well along the first axis (Fig. 2a). Isoeto lacustris-sparganietum borderei (group A) is located between Sparganio angustifolii-isoetum echinospori (group B) and Sparganio angustifolii-callitrichetum font-queri (group C). Fig. 2b shows that the species closest to the centre of the three groups are Sparganium angustifolium, the only one present in all the releves, and Subularia aquatica, which is common to all the groups. The isoetids are the main elements in the differentiation ofthe groups, in which the accompanying phytogeographic element also varies. Thus, while the boreal element is predominant in group A, in group B the influence of the Ibero-Atlantic element starts to be seen (e.g., Baldellia alpestris). In group C the presence of the Ibero-Atlantic element is notable and implies the existence of taxa which characterizeboth the submergedlayer (lsoetes velatum) and the layerwith floating leaves (Antinoria agrostidea subsp. natans). Finally, axis 2, along which group A corresponding to the Isoeto lacustris-sparganietum borderei association - is spread, seems to bear some relationship to water depth.
5 Littorellion in Spain 257 s- 4 a CA for samples 3 A N /Jl ~ 2-1 J C t::. t::. B ~~t::. of:bqdjo.,& t::. t::. t::. i J 6, OD Axis b + Iso lac CA for plants 2 N /Jl ~ llllqo Spaang" SO 11<11 Iso ech + Iso vel + ell \ Ill\> -1 \,.i\ llc'i Axis 1 Fig. 2. CA ordination analysis of46 Littorellion releves from Spain. Groups correspond to those ofclassification analysis. a - CA ordination for samples; b - CA ordination for plants. Summary information ofca: eigenvalues: axis I =.612, axis 2 =.496, cumulative percentage of variance: axis I = 14.4, axes 1+2 =26.. Ant nat Antinoria natans, Bal alp - Baldellia alpestris, Iso ech - Isoetes echinosporum, Iso lac - I. lacustre, Iso vel - I. velatum, Lit uni - Littorella uniflora, Spa ang - Sparganium angustifolium, Sub aqu - Subularia aquatica.
6 258 J.A. Molina et al. Table 2. Phytogeographical groups ofthe flora characterizing Littorelllion alliance in the Spanish high-mountain ranges. Boreal-alpine taxa Taxa endemic to the Iberian Peninsula Boreal-Atlantic taxa lsoetes echinosporum, lsoetes lacustre, Sparganium angustifolium, Subularia aquatica Antinoria agrostidea subsp. natans, Baldellia alpestris, lsoetes velatum subsp. asturicense, lsoetes velatum subsp. velatum f. lereschii Littorella unijlora Phytogeographical groups Two major phytogeographical groups can basically be recognized within the flora characterizing the Littorellion alliance in the Iberian Peninsula (Tab. 2). The first includes the boreal-alpine taxa found throughout the Spanish high-mountain ranges and whose presence gradually decreases from north to south and from east to west. The second includes taxa which are endemic to the north-western mountains ofthe Iberian Peninsula and whose presence increases in inverse proportion to that of the first group. Examination of the taxa in each group reveals that while the northern group consists of taxonomically well-defined species, the western group contains taxa of an infraspecific rank. (Antinoria agrostidea subsp. natans, lsoetes velaturn subsp. asturicense, lsoetes velaturn subsp. velaturn f. lereschii) which are closely related to more widespread lowland taxa (Antinoria agrostidea subsp. agrostidea, lsoetes velaturn subsp. velaturn f. velaturn). This seems to indicate that the origin of these microtaxa lies in plants which originally grew throughout the western half of the Iberian Peninsula and probably adapted to colder habitats than those that their predecessors had, and which are today relegated to the western Spanish high-mountain ranges. Syntaxonomical synopsis Class: Littorelletea unijlorae BRAUN-BLANQUET & TDXEN ex WESTHOFF et al Order: Littorelletalia W. KOCH 1926 Alliance: Littorellion unijlorae W. KOCH 1926 Association: lsoeto lacustris-sparganieturn borderei BRAUN-BLANQUET 1948 Association: Sparganio angustifolii-lsoeteturn echinospori RIVAS-MARTINEZ & G. NAVARRO in G. NAVARRO 1987 Association: Sparganio angustifolii-callitricheturn font-queri RNAS GODAY & RNAS-MARTINEZ 1959 Association: Isoeto lacustris-sparganietum borderei BRAUN-BLANQUET 1948 Synonym: lsoeteturn brochonii DIERSSEN 1975 BRAUN-BLANQUET (1948) consideredi. brochonii to be a characteristic species ofthelsoeto lacustris-sparganieturn borderei association. Furthermore, lsoetes brochonii which is recordedly confined to about 16 high-mountain lakes in the eastern Pyrenees (COOK 1983), is considered as possibly a variant oflsoetes lacustre, according to JERMY & AKEROYD (1993). For all of these reasons, the lsoeteturn brochonii, also described from the Pyrenees (DIERSSEN 1975), is a syntaxonomical synonym of the lsoeto lacustris-sparganieturn borderei (art. 22, BARKMAN et al. 1986).
7 Littorellion in Spain 259 Association: Sparganio angustifolii-isoetetum echinospori RIVAS-MARTINEZ & G. NAVARRO in G. NAVARRO 1987 Synonym: Isoeto-Sparganietum borderei auct. In some Pyrenean lakes Isoetes lacustre frequently grows with Isoetes echinosporum (BUADES & PRADA 1992), even though the two species seem to occupy different ecological niches: I. lacustre grows in deep waters, while I. echinosporum develops in shallower waters (RIVAS-MARTINEZ et al. 1991). Furthermore, both species have different bioclimatic ranges: alpine in the case of I. lacustre and subalpine in the case of I. echinosporum (CARRILLO & NINOT 1992). These facts lead us to identify two different associations in the Pyrenean area; one floristically characterized by I. lacustre and the other by I. echinosporum. Though the Sparganio angustifolii-isoetetum echinospori association seems to be very close to the Isoetetum echinospori W. KOCH 1926 association, the latter incorporates Ranunculus reptans which does not occur in the mountains of southern Europe. Association: Sparganio angustifolii-callitrichetum font-queri RIVAS GODAY & RIVAS-MARTINEZ 1959 Synonyms: Sparganieto (borderei)-isoetetum boryanae RIVAS-MARTINEZ 1963; Sparganio-Isoetetum velatae RIVAS-MARTINEZ 1963 corr. RIVAS-MARTINEZ & G. NAVARRO 1987 in G. NAVARRO 1987; Subulario aquaticae-isoetetum asturicensis F. NAVARRO et al. ex RIVAS-MARTINEZ & G. NAVARRO in G. NAVARRO The references of the Iberian System's Callitriche' obtusangula and C. hamulata (NAVARRO 1987) were discarded, while the references of the Cantabrian C. font-queri (RIVAS GODAY & RIVAS-MARTINEZ 1959) have been considered as synonym to C. platycarpa (SCHOTSMAN 1967). Three different associations have been described in the Hesperian Massif: one in the Cantabrian Mountains (Sparganio angustifolii-callitrichetum font-queri), another in central Sierra de Gredos (Sparganio-Isoetetum boryanae) and a third in western Sierra de Gredos (Subulario aquaticae-isoetetum asturicensis). This analytical viewpoint has been based on the occurrence of both differential I. velatum microtaxa and some non-faithful Littorelletea taxa. While authors accept the I. velatum microtaxa which have been described (PRADA 1983, PRADA 1986), a synthetic approach with only one association characterized by Isoetes velatum sensu lato seems to be more proper to make all Spanish associations comparable with each other and to explain their phytogeographical significance. Acknowledgements: We would like to thank Professors Jesus Izco and Federico Femandez and the three anonymous referees for their contributions which have greatly improved the manuscript. This research was supported by COMPLUTENSE project PR49/ REFERENCES BARKMAN J.J., MORAVEC J. & RAUSCHERT S. (1986): Code ofphytosociological nomenclature. Vegetatio 67: BRAUN-BLANQUET J. (1948): la vegetationalpinedes Pyreneesorientales. Etude de phytosociologie comparee. Monogr. Estac. Estud. Pirenaicos, Barcelona. BRAUN-BLANQUET J. (1979): Fitosociolog a. Bases para el estudio de las comunidades vegetales. Blume, Madrid. BUADES A. & PRADA C. (1992): Cartograffa Corol6gica Iberica. Aportaciones 3 y 32. Bot. Complut. 17:
8 26 J.A. Molina et al. CARRILLO E. & NINOT J.M. (1992): Flora i vegetaci6 de les valls d'espot i de Boi (Flora and vegetation of the Espot and BOI valleys). Arxivs Secc. Ci. Inst. Estud. Catalans 99(1-2). CASTROVIEJO S., L~fNz M., L6PEZ GoNzA.LEZ G., MONTSERRAT P., MUNoZ GARMENDIA F., PAIVA J. & VILLAR L. (eds.) ( ): Flora iberica 1-5,8. CSIC, Madrid. COOK C.D.K. (1983): Aquatic plants endemic to Europe and the Mediterranean. Bot. Jahrb. Syst. 13: DEN HARTOG C. & SEGAL S. (1964): A new classification of the water plant communities. Acta Bot. Neerl. 13: DIERSSEN K. (1975): Littorelletea uniflorae. Prodromus der europiiischen Pflanzengesellschaften, Lfg. 2. Cramer. Vaduz. DUFRENE M. & LEGENDRE P. (1991): Geographic structure and potential ecological factors in Belgium. J. Biogeogr. 18: JERMY A.C. & AKEROYD J.R. (1993): Isoetes L. In: TullN T.G. etal. (eds.), Flora europaea 1, Ed. 2, Cambridge University Press, Cambridge. NAVARRO F., SANCHEZ J.A. & VALLE CJ. (1979): Comentarios florlsticos y ecol6gicos sobre Subularia aquatica L. Publ. Dep. Bot. Fac. Fann. Salamanca 1: NAVARRO G. (1987): Datos sobre la vegetaci6n acmitica de las lagunas glaciares de Urbi6n y Neila (Soria-Burgos). Lazaroa 7: OBERDORFER E. (1977): Suddeutsche Pflanzengesellschaften I. Ed. 2, Fischer, Stuttgart, New York. PIETSCH W. (1971): Beitrag zur Soziologie und Okologie der europaischen Littorelletea- und Utricularietea-Gesellschaften. Feddes Repert. 88: PODANI J. (1993): SYN-TAX-pc. Computer programsfor multivariate data analysis in ecology and systematics. Version 5.. Scientia Publishing, Budapest. PRADA C. (1983): El genero Isoetes L. en la Peninsula Iberica. Acta Bot. Malac. 8: PRADA C. (1986): Isoetes L. In: CASTROVIEJO S. et al. (oos.), Flora iberica 1, CSIC, Madrid, pp RIVAS GoDAY S. & RIvAs-MARTINEZ S. (1959): Una visita a la Laguna de Arvas (Leitariegos). Anales Inst. Bot. Cavanilles 16: RIVAS-MARTfNEZ S. (1%3): Estudio de la vegetaci6n y flora de las sierras de Guadarrama y Gredos. Anales Inst. Bot. Cavanilles 2: RIVAS-MARTfNEZ S., BAcONES J.c., DfAZ T.E., FERNANDEZ-GoNZALEZ F. & LOIDI J. (1991): Vegetaci6n del Pirineo occidental y Navarra. Itinera Geobot. 5: SCHAMINEE J.HJ., WESTHOfF V. & ARTS G.H.P. (1992): Die Strandlinggesellschaften (Littorelletea BR.-BL. et Tx. 43) der NiOOerlande, in europaischem Rahmen gefasst. Phytocoenologia 2: SCHAMINEE J.HJ., WEEDA EJ. & WESTHOfF V. (1995): De Vegetatie van Nederland 2. Plll!l1engemeenschappen van wateren, moerassen en natte heiden (The vegetation ofthe Netherlands 2. Plant communities ofwater bodies, swamps and wet heathlands). Opulus, UppsalalLeiden. SCHOTSMAN D.H. (1967): Les Callitriches. Especes de France et taxa noveaux d'europe. Centre National de Floristique du C.N.R.S, Paris. TER BRAAK C,J.F. (1985): Canoco -a FORTRAN program for community ordination by [partial] [detrented] [canonical] correspondence analysis, principal components analysis and redundance analysis. Versiun 2.1. ITI-TNO, Wageningen. TUTlN T.G. et al. (OOs.) ( ): Flora europaea 1-5. Cambridge University Press, Cambridge. VAN DER MAAREL E. (1979): Transformation of cover-abundance values in phytosociology and its effects on community similarity. Vegetatio 39: Received 23 February 1998, revision received 17 February 1999, accepted 15 March 1999
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