Wealth of Flora and Vegetation in the La Campana-Peñuelas Biosphere Reserve, Valparaiso Region, Chile

Chile has a National System for State-Protected Wilderness Areas (Sistema Nacional de Areas Silvestres Protegidas del Estado – SNASPE), which consists of three categories: National Parks (PN), National Reserves (RN) and Natural Monuments (MN). It presently contains 95 units, covering in total 19% of the country's territory. SNASPE has become a fundamental pillar not only for safeguarding an important part of Chile's natural heritage but also for protecting and valuing our cultural heritage, particularly where it is integrated in the areas which make up this system (Oltremari, 2002). By 1985, UNESCO had designated 7 Biosphere Reserves in Chile: Lauca, Fray Jorge, Juan Fernandez, La Campana-Penuelas, Araucarias, Laguna San Rafael and Torres del Paine. To these were later added Cabo de Hornos [Cape Horn], Bosques Templados Lluviosos de los Andes [Wet Temperate Andean Forests], and recently Laguna del Laja-Nevados de Chillan.

The identification, nomenclature and geographical origin of each species was based on Muñoz (1966), Navas (1973Navas ( , 1976Navas ( , 1979)), Hoffmann (1978Hoffmann ( , 1991)), Marticorena & Quezada (1985), Matthei (1995), Hoffmann et al. (1998) and Marticorena & Rodríguez (1995, 2001, 2003, 2005).The International Plant Names Index (IPNI 2011) was used to update the scientific names and abbreviations.Life forms were determined according to the scheme proposed by Ellenberg & Mueller-Dombois (1966) and the state of conservation of the species was determined considering the proposals of Benoit (1989), updated by a meeting of experts in September 1997 (Baeza et al., 1998;Belmonte et al., 1998;Ravenna et al., 1998), and de Novoa et al. (2006) for the Orchidaceae.The degree of human disturbance of the site was determined on the basis of the proposal of Hauenstein et al. (1988) and the evaluation scale of González (2000), which consider phytogeographic origin (the ratio between native and introduced species), and life forms (Raunkiaer's biological forms) as measurements of this form of disturbance.The result was an inventory of the flora in the study area (table 2), containing all the above elements.
The vegetation units were determined using the maps produced by CONAF & CONAMA (1999) and specific cartography provided by CONAF (National Forest Corporation), Valparaiso Region.The definition and nomenclature of the vegetation units followed the proposal of Gajardo (1995).The vegetation units identified in the map for study were subsequently verified on the ground.
Vegetation.The vegetation in the Reserve includes the following woody communities: sclerophyllous forest, hygrophilous forest, deciduous forest, thorny scrub and mixed sclerophyllous scrub.The herbaceous communities include: dry grassland, wet grassland, reed beds, sedge beds and the aquatic plant community.These communities are characterised as: 1. Peumo and boldo sclerophyllous forest.This is a woody formation typical of the region.
This community corresponds to Peumo-Cryptocaryetum albae (Oberdorfer, 1960).Variants can be found with sclerophyllous scrub species (Retanilla trinervia, Gochnatia foliolosa), and one with Chilean palm tree (Jubaea chilensis).The average cover of the arboreal stratum is 70%, shrubs 35% and herbaceous 25%.The principal arboreal species are: Cryptocarya alba, Peumus boldus, Persea lingue and Dasyphyllum excelsum; shrubs are dominated by: Retanilla trinervia, Schinus latifolia and Chusquea cumingii,; creepers and lianas included: Proustia pyrifolia, Lardizabala funaria and Cissus striata; herbaceous vegetation comprised mainly: Blechnum hastatum, Alonsoa meridionalis, Conyza floribunda and Anagallis arvensis.The altitude ranges of this community is from 350 to 1,000 masl (Elórtegui & Moreira, 2002;Hauenstein et al., 2009 The altitude range is from 500 to 1,050 masl.There is also a variant with Jubaea chilensis, in which Aristeguietia salvia and Acacia caven are also present (Elórtegui & Moreira, 2002;Hauenstein et al., 2009).(Ramírez et al. 1996).These forests are included in the Wintero-Nothofagetea phytosociological class defined by Oberdorfer (1960).Other woody species present in this community were: Maytenus boaria and Escallonia revoluta, together with some creepers such as Cissus striata and Lardizabala biternata.The herbaceous stratum is scarce, probably due to the closed canopy, which hinders the penetration of light; where present it is represented by Uncinia trichocarpa and ferns like Blechnum hastatum and B. cordatum.This community is found at 270 masl (Hauenstein et al., 2009).4. Belloto hygrophilous laurifolious forest.This community is characterised by an arboreal stratum dominated by Beilschmiedia miersii, Cryptocarya alba and Dasyphyllum excelsum; there is an abundant shrub stratum dominated by Azara celastrina, Chusquea cumingii, Adenopeltis serrata and an abundance of creepers such as Proustia pyrifolia, Lardizabala funaria and Bomarea salsilla.It is found in low-lying areas, up to 500 masl (Elórtegui & Moreira, 2002). 5. Canelo hygrophilous laurifolious forest.The arboreal stratum, dominated by Drimys winteri; an abundant shrub stratum, with Otholobium glandulosum, Escallonia myrtoidea, Maytenus boaria and occasionally Salix humboldtiana; and in the herbaceous stratum, Equisetum bogotense.In altered sectors by human activities, cover may be diminished to as little as 30%.It is found at between 500 and 1,300 masl (Elórtegui & Moreira, 2002).6. Deciduous roble forest.This community is characterised by a well differentiated arboreal stratum with Nothofagus macrocarpa and Lomatia hirsuta; a shrub stratum with Azara petiolaris, Ribes punctatum, Schinus montanus, Berberis actinacantha and Aristotelia chilensis; and an herbaceous stratum with, Adiantum sulphureum, Loasa tricolor, Oxalis laxa and Alstroemeria zoellneri, respectively.The cover is from 70 to 100% and it is found between 1,100 and 1,500 masl.At altitudes above 1,500 masl, a clear diminution may be seen in the tree and shrub cover, constituting a variant with other species such as Schizanthus hookeri, Valeriana lepidota and Senecio anthemidiphyllus (Elórtegui & Moreira, 2002) (photo 4).accompanied by shrub forms of Lithrea caustica and Quillaja saponaria, and by Cuscuta chilensis, an abundant, parasitic, herbaceous species.Average cover is above 70% and the community is found between 400 and 1,000 masl.It forms a variant with abundant presence of Jubaea chilensis, but only in the Ocoa sector (Elórtegui & Moreira, 2002).(Elórtegui & Moreira, 2002).14.Dry grassland.The principal floral components of these grasslands were Phyla canescens, Bromus hordeaceus, Agrostis capillaris, Hypochaeris radicata, Gamochaeta coarctata, Leontodon saxatilis, Rumex acetosella and Avena barbata.They correspond to the Bromo-Lolietum community (Oberdorfer, 1960), and are found in the north-east sector of Peñuelas lake, at around 360 masl (Hauenstein et al., 2009).15-16.Wet grasslands.There are two types.Apart from some of the species of the previous community, the first is distinguished by Mentha pulegium and reeds (Juncus acutus, J. cyperoides, J. pallescens), and corresponds to reedy wet grassland (Juncetum acuti ass.nov.).The second has marked presence of Ludwigia peploides, Cotula coronopifolia, Distichlis spicata and Paspalum dilatatum, corresponding to Polygono-Ludwigietum peploidis (Steubing et al. 1980).Both are found on the northern and southern plains close to Peñuelas lake, although Polygono-Ludwigietum occupies the strip closest to the water (Hauenstein et al., 2009).17-18.Marsh communities.Two communities of marsh plants were identified, preferably located near the channel which flows into the eastern end of Peñuelas lake.The first, located closer to the water, corresponds to Scirpetum californiae (Ramírez & Añazco, 1982), the principal component being totora reed (Schoenoplectus californicus), accompanied by Ludwigia peploides and Polygonum hydropiperoides.The second community, found in a continuous strip a little further away from the water, corresponds to Loto-Cyperetum eragrostidae (San Martín et al., 1993), the principal species being Cyperus eragrostis and Carex excelsa (saw-sedges), accompanied by Juncus pallescens and J. acutus; it is a perennial, marshy association, typically found in depressions and on the banks of watercourses, associated with totora reeds or the border of swamp forest with temo (Blepharocalyx cruckschanksii) and pitra (Myrceugenia exsucca) (Hauenstein et al., 2002;San Martín et al., 2002).In both communities (reed beds and sedge beds), due to the periodic flooding of the site, hydrophytic life forms dominate absolutely, such as typical helophytes (marsh or swamp plants) and hydrophytes (Hauenstein et al., 2009).19.Aquatic communities.These communities consist principally of hydrophytic species, particularly Azolla filiculoides, a free-floating pteridophyte, constituting the Lemo-Azolletum filiculoidis association (Roussine & Negre, 1952); moreover the high frequency of Hydrocotyle ranunculoides, H. modesta and Eleocharis exigua allow the existence of Hydrocotyletum to be inferred (San Martín et al., 1993), however more censuses would be required to confirm this inference.For example, in the least overgrown part of the spring in the El Abrevadero sector of RN Lago Peñuelas, a small body of water is formed which is colonised by aquatic and marsh species such as: Azolla filiculoides, Gunnera tinctoria, Juncus cyperoides, Carex excelsa, Eleocharis exigua, Polygonum hydropiperoides, Hydrocotyle modesta and H. ranunculoides (Hauenstein et al., 2009).

EC Bibliographical source
To resume, without considering the variants, 19 plant associations have been described for the Biosphere Reserve.

Discussion
Flora.When the general floral wealth of the area (420 species) is compared with other surveys done in protected wilderness areas in central Chile, we find for the Maule Region: RN Los Bellotos del Melado -297 species (Arroyo et al., 2000); RN Los Ruiles -139 species; RN Los Queules -104 species (Arroyo et al., 2005).For the Metropolitan Region: Monumento Natural El Morado -300 species (Teillier, 2003); RN Río Clarilloapproximately 600 species (Teillier et al., 2005).With the exception of the last, all others consist of considerably fewer species than recorded in the La Campana-Peñuelas Biosphere Reserve, demonstrating the floral wealth of this area.
The biological spectrum shows the predominance of therophytes, hemicryptophytes and cryptophytes over other life forms, which is consistent with the xeric conditions of the site, especially during summer, since therophytes (herbaceous plants with short life cycles, annuals or biannuals) and cryptophytes (geophytes or plants with enduring subterranean organs) represent this type of climate very well and are good environmental indicators.Meanwhile the abundance of hemicryptophytes is indicative of human intervention, since this life form accompanies man and corresponds to plants capable of surviving being trodden on and browsed by domestic animals (Cabrera & Willink, 1973;Ramírez, 1988;Grigera et al., 1996).
The general phytogeographic origin of the plants in the Reserve indicates that 23% are introduced species, 49% native and 28% endemic.This confirms the high value of this Biosphere Reserve as an area for the conservation of Chile's native and endemic flora.At the same time, when the relatively high percentage of allochthonous species is considered, and compared to the majority of the studies mentioned above where the values for allochthonous species do not exceed 20%, this would indicate a high level of human intervention in the study area.According to Hauenstein et al. (1988) and González (2000), a percentage distribution in which allochthonous plants reach values of between 20 and 30% corresponds to the category of "moderate intervention".This high level of intervention is explained by the large flow of visitors and the presence of domestic animals at certain times of year, leading to the arrival of therophytes and hemicryptophytes which, as mentioned previously, correspond for the most part to fast-growing and strongly invasive plants.To this must be added the different soil structure in some sectors of RN Peñuelas under plantations of exotic species (Pinus radiata, Eucalyptus globulus) and the aggressive colonization by Australian acacias (Acacia dealbata, A. melanoxylon) (ICSA, 1980;CONAF, 1994).Arroyo et al. (1995) indicate that the high percentage of endemic species is remarkable in all the protected wilderness areas of Chile's central zone, with values over 40%, which rise to 70% when native plants are included; introduced species thus do not exceed 30%.This is one of the characteristics which highlight the value of these areas as sites where our flora and vegetation units are preserved and protected (Luebert & Becerra, 1998;Hauenstein et al., 2009).
The high number of monocotyledons in the sector should also be noted, especially the abundance of bulb geophytes, which include the majority of species with conservation problems.It should be born in mind that these bear beautiful, brightly coloured flowers, and are especially important in the Bajo Los Lirios sector (CONAF, 1994(CONAF, , 2008;;Hauenstein et al., 2009), where there are very brightly coloured and varied Orchidaceae, the Iridaceae, with lilies of the genera Sisyrinchium and Olsynium, and the tahay (Calydorea xiphioides) an "endangered" species which is very scarce throughout the central zone.There are other more frequent but no less beautiful species, like the lahue (Herbertia lahue), and flowers of the genera Alstroemeria, Phycella, Rhodophiala and Calceolaria, which are of aesthetic importance for recreation and use in gardening (Riedemann & Aldunate, 2001;Muñoz & Moreira, 2002).
Vegetation.The total phytosociology of the site consists of 19 plant associations, 6 of which are herbaceous, 7 scrub and 6 forest.With respect to the open espino scrub, also known as "espino or acacia steppe" (Pisano, 1956;CONAF, 1994), it should be made clear that strictly speaking it is not steppe but rather a savannah, as stated by Grau (1992), since the term steppe covers isolated vegetation with denuded surrounding soil and represents cold environments.Savannah on the other hand has isolated trees or thorny shrubs and a rich herbaceous stratum (Cabrera & Willink, 1973).This herbaceous stratum rich in forage species allows use of this type of community, at certain times of year, for grazing by domestic animals in RN Lago Peñuelas; this activity needs to be reviewed urgently by CONAF, since its effects on the biodiversity of the site are unknown.
The predominance of therophytes and geophytes in the biological spectrum of this plant formation is consistent with the climatic conditions and levels of precipitation in the area, since these life forms present morphological and physiological adaptations to the environmental conditions with extended periods of drought, and they are also important elements as food for wild fauna.The lower percentage of phanerophytes is explained by the low levels of precipitation in the area, and probably also the felling of native woody vegetation in the past.The scarcity of chamaephytes is due to the fact that this life form is adapted to conditions of low temperatures and greater altitude, such as are found only on El Roble and La Campana mountains (Cabrera & Willink, 1973;Ramírez, 1988;Grigera et al., 1996).
In the mixed sclerophyllous scrub, the important forms are the sclerophyllous phanerophytes and the therophytes; this also indicates the suitability of this type of plant formation to the climatic conditions of the area.The strong presence of hemicryptophytes indicates human alteration (Hauenstein et al., 1988).Numerous authors have carried out ecophysiological studies on mediterranean scrub species, explaining their ability to adapt to this type of environment, including Mooney & Kummerow (1971) on the drought response of Flourensia thurifera, Kageneckia oblonga, Lithrea caustica and Proustia cinerea; Montenegro et al. (1979) on the growth dynamic of Colliguaja odorifera, Lithrea caustica, Satureja gilliesii and Retanilla trinervia; Araya & Avila (1981) on the production of new shoots in scrub species affected by fire; and Avila et al. (1981) on the behaviour of herbaceous stratum species in scrub after a fire.
With respect to sclerophyllous forest, the predominance by phanerophytes and the importance of therophytes and hemicryptophytes are also consistent with the mediterranean climate of the area, since the species present adaptations which enable them to survive intense water stress, e.g. the presence of sclerophyllous leaves (Mooney & Kummerow, 1971), and the fires which are frequent in the area.For protection against fire, many develop a thick peridermis or a lignotuber, structures which enable them produce new shoots after a disaster (Araya & Avila, 1981).This community was classified by Oberdorfer (1960) in the class Lithraeo causticae-Cryptocaryetea albae and extends from 31° South to the limit of temperate territory (Aguilella & Amigo, 2001).There is no doubt that areas with this type of vegetation have been most affected by human action (Balduzzi et al., 1981(Balduzzi et al., , 1982)).
At the same time, the remnants of hygrophilous forest, which requires conditions of greater humidity and precipitation, present absolute predominance of phanerophytes and nanophanerophytes (shrubs) over other life forms, indicating that the area would present high levels of rainfall, which is not the case.The explanation of the presence of this forest with hygrophilous characteristics at the site is based on the fact that it grows above a spring located in the Vega del Álamo sector, also known as the "abrevadero de caballos" [horse water-hole], which generates abundant water all year round, maintaining this community with azonal characteristics (Ramírez et al., 1996;Hauenstein et al., 2009).
The dry grassland is characterised by the predominance of hemicryptophytes, indicating strong human action, since these life forms are adapted to survive being trodden on and browsed by animals introduced by man; and of therophytes, indicating drought conditions (Hauenstein et al., 1988;Ramírez, 1988).In the wet grassland on the other hand, cryptophytes and hemicryptophytes predominate.
Reed beds are the most abundant and variable marsh associations in central-southern Chile, colonising marshes and banks of shallow lotic and lentic bodies of water (Ramírez & Añazco, 1982;Ramírez et al., 1987;San Martín et al., 1993).The same is true of sedge beds, which habitually accompany reed beds, forming a characteristic drier fringe.The principal species, Cyperus eragrostis and Carex excelsa, have sharp-edged leaves, from which their common name of "saw-sedges" derives (Hauenstein et al., 2002(Hauenstein et al., , 2005a)).
The hydrophyte community corresponds to Lemno-Azolletum, characteristic of eutrophied aquatic environments (Palma et al., 1978); it is mentioned by Ramírez et al. (1987) as very abundant in lakes in Chile's central zone.Likewise, species such as Hydrocotyle modesta and H. ranunculoides are indicators of organic contamination with nitrogen (Hauenstein et al., 2005b), which would corroborate the high trophic levels of Peñuelas lake; at the same time, this body of water and its associated flora form the habitat for a rich avifauna (Strang, 1983).
In this respect, Arroyo et al. (2005) propose, among other measures, the urgent need to complete inventories of flora of all the protected areas of central Chile; likewise they suggest analysing these areas at the scale of small polygons to evaluate their biological importance and vulnerability, elements which should form the basis for an integrated conservation strategy.Likewise, the findings of Armesto et al. (2002) and Simonetti (2004) are important, regarding the need to increase the number of protected areas, both public and private, to increase the size of existing areas, and to make use of the environment which surrounds them and which has suffered intervention, in order to create interconnectivity zones between them to serve as biological corridors.These units of conservation should consider representation of the different types of vegetation (Luebert & Becerra, 1998).Another interesting proposal is that of Elórtegui & Moreira (2002) for La Campana National Park, to zone areas for different types of use.In this context, Simonetti (1995) proposes the need for a model for planning the organization of these protected areas, linking the need to conserve natural resources with their sustainable use, which would be a basic support tool for defining which, where and how possible activities could be carried out, in such a way as would be compatible with conserving biodiversity.

Conclusions
The study reported here of the La Campana-Peñuelas Biosphere Reserve registered 420 species of vascular plants, of which 49% are of native origin, 28% correspond to endemic species and 23% to introduced species, respectively.Taxonomically, they are divided into 12 Pteridophytes, 3 Gymnosperms, 290 Dicotyledons (Magnoliopsida) and 115 Monocotyledons (Liliopsida), representing a high floral wealth.However, the percentage of allochthonous plants indicates a moderate degree of human disturbance.Eighteen species present conservation problems (2 Endangered, 13 Vulnerable, 2 Rare, 1 Insufficiently known).The vegetation at the site includes the presence of 19 plant communities, six of which are herbaceous, seven shrub and six arboreal.Important sectors exist of standing out in the Reserve such as: Los Lirios sector, which contains a high percentage of bulb species and numerous threatened species; the Vega del Álamo sector as a valuable remnant of hygrophilous forest; and the Ocoa sector due to the important presence of the endemic Chilean palm tree (Jubaea chilensis).

Acknowledgements
Thanks to the staff and park wardens of CONAF, Valparaiso Region, for their support in field activities and for facilitating the photographies, bibliographic and cartographic information.

Photo 4 .
Photo 4. Nothofagus macrocarpa forest in the sector of the Hill the Oak. 7. Espino thorny scrub.The dominant species in the community are espino (Acacia caven = Vachellia caven) and maitén (Maytenus boaria), with average cover of 50% and 10% respectively.It is characterised by the presence of a rich herbaceous stratum, especially Agrostis capillaris, Leontodon saxatilis, Avena barbata, Bromus hordeaceus, Briza minor, B. maxima and Rhodophiala advena, with clear predominance of forage graminids.This community is found around Peñuelas lake (Hauenstein et al., 2009) (photo 5).8. Trevo thorny scrub.A little developed shrub community dominated by Retanilla trinervia,accompanied by shrub forms of Lithrea caustica and Quillaja saponaria, and by Cuscuta chilensis, an abundant, parasitic, herbaceous species.Average cover is above 70% and the community is found between 400 and 1,000 masl.It forms a variant with abundant presence of Jubaea chilensis, but only in the Ocoa sector(Elórtegui & Moreira, 2002).

Table 1
. Vascular plants with conservation problems of the La Campana-Peñuelas Biosphere Reserve (EC= condition of conservation, P= threatened, R= rare, V= vulnerable, IC= insufficiently known).3. Temo and pitra hydrophilous laurifolious forest.Includes small remnants of forest associated with permanent watercourses and springs, present in the Vega del Alamo sector of RN Peñuelas.These are composed of hygrophilous species such as Drimys winteri, Myrceugenia obtusa, Blepharocalyx cruckshanksii and Luma chequen, and some creepers like Lardizabala biternata and Cissus striata, and correspond to the Blepharocalyo-Myrceugenietum exsuccae association (hualve or swamp forest) of myrtaceous plants in the central southern zone of Chile