Composition, ecology and conservation of the south-Iberian serpentine flora in the context of the Mediterranean basin

Abstract


INTRODUCTION
Peridotites are recognized as one of the most peculiar rock types on Earth, both for their plutonic igneous origin and chemical composition (Roberts & Proctor, 1992).Serpentine soils originate from this type of rock, and are well known for their physical and chemical anomalies that present a hostile environment for plants (Brooks, 1987).Anomalies such as high Fe and Mg contents, a low Ca content, a deficiency of nutrients (N, P, K), infertility, toxic concentrations of heavy metals (Cr, Ni, Co, Va), very slow soil development and high xerothermicity characterize these soils (Whittaker, 1954;López González, 1975;Brooks, 1987).Such characteristics make serpentine habitats highly selective for plants and relatively few species, called serpentinophytes or serpentino philous, are adapted to grow on such a substrate (Rune, 1953;Jeffrey, 1987;Selvi, 2007).Following Kruckeberg (2002), serpentino-phytes can be divided into three categories: a) endemic taxa, linked exclusively to peridotites, b) preferential taxa, whose distribution is mainly associated with peridotite but occasionally found on other substrata and c) taxa living on a variety of substrata but also on peridotite (bodenvag taxa).
Obligate serpentinophytes may have a particular metabolism for avoiding the toxic effect of heavy metals (Roberts & Proctor, 1992;Brady & al., 2005).Moreover, some facultative species show a serpentine-morph syndrome, e.g. a complex of morpho-functional adaptations that distinguish the serpentine populations from those living on other substrates (stenophyllous, glabrous, glaucous, macro-rooted plants, plagiotropism and nanism) (Pichi-Sermolli, 1948).The high concentrations of magnesium in serpentine soils allow the presence of a magnesicolous flora that develops equally on serpentine and dolomite rocks (Rivas Goday, 1974;Mota & al., 2008).Studies on species adapted to this type of serpentine Composition, ecology and conservation of the south-Iberian serpentine flora in the context of the Mediterranean basin Andrés V. Pérez-Latorre, Noelia Hidalgo-Triana* & Baltasar Cabezudo Departamento de Biología Vegetal (Botánica), Universidad de Málaga, P. O. Box 59, E-29080 Málaga, Spain avperez@uma.es;nhidalgo@uma.es;bcabezudo@uma.esecosystem are considered of great interest for the restoration of contaminated soils, the mining of heavy metals, the study of the evolution in extreme habitats, and in conservation biology surveys (Brady & al., 2005).
The most important area for obligate serpentinophytes in Europe (with 123 taxa) is situated in the Balkans (Stevanovic & al., 2003).The westernmost peridotite outcrops in the Mediterranean Basin are situated in the south of the Iberian Peninsula (Andalusia) where they cover a total area of 430 km 2 (IGME, 1970 and1981), with an altitudinal range from 100 to 1500 m occupying three bioclimatic belts (Pérez Latorre & al., 1998).South-Iberian peridotites have frequently been converted into serpentines by hydrolysis (Yusta & al., 1985).
The flora and plant communities of Andalusian peridotites have been studied by several authors, including Rivas Goday (1974), López González (1975) and Rivas Goday & López Gon zález (1979).Some species are hyper-accumulators of Ni (Rufo & al., 2004;Díez-Garretas & al., 2009) and others show the serpentine-morph syndrome characters described above (López González, 1975;Alados & al., 1999).Climax forest vegetation in these habitats is characterized by pine (Pinus pinaster Aiton) and fir forest (Abies pinsapo Clemente ex Boiss.) but they are frequently substituted by shrublands because of frequent fires (Cabezudo & al., 1989;López González, 1975;Pérez Latorre & al., 1998).Most south-Iberian serpentinophytes and the plant communities where they live are included in the 92/43EU "Habitats" Directive; some of them are also threatened and/or protected.Some of the peridotite outcrops are listed as LIC (Important Areas for European Conservation) and/or regional protected areas (Natural Park, Natural Site) and they are considered as Mediterranean phylogeographic refuges and "hot-spots" for Mediterranean plant diversity (e.g.part of the Serrania de Ronda refugia; Médail & Diadema, 2009).They are also considered important areas (exceptional category) for threatened Spanish flora (Bañares & al., 2003).Moreover, peridotite outcrops have a great importance in the phytogeographical scheme of the Iberian Peninsula as they are given the category of sector (Bermejense sector) within the Betica province (Western Mediterranean region) (Nieto & al., 1991).In an attempt to broaden our knowledge of peridotite plant biology and distribution, the main aims of this work were to: 1, provide a checklist of the serpentinophytes of the southern Iberian Peninsula; 2, study serpentinophytes as a group in terms of life form, systematic spectrum (families), ecology, phytosociology and threat level; and 3, compare the group of south-Iberian serpentinophytes with other Mediterranean serpentine floras and the flora living on other closely related rocks such as dolomites.

Study area
The main peridotite outcrops in the south of the Iberian Peninsula (Fig. 1) are located in the province of Malaga (Ronda Mountain Range; Fig. 2).The mineralogical composition is characterized by harzburgite, lherzolite, piroxenite and serpentinite.They can be grouped them into four geographical units (Fig. 2): 1, Sierra Bermeja: the most important outcrop, covering 319 km 2 with an altitude range of between 50 and South-Iberian serpentinophytes 1500 m. 2, Sierra Alpujata: 71 km 2 with an altitude range of between 140 and 1050 m. 3, Sierra de Aguas: 36 km 2 and lying between 200 and 950 m. 4, Sierras del Guadalhorce: small and isolated outcrops with a total area of 6 km 2 and altitude range between 100 and 400 m.

Serpentinophytes checklist
The list of species to be included as serpentinophytes has been created based in several sources.We follow the criteria used by Mota & al. (2008Mota & al. ( , 2011) ) to select taxa associated with special substrata, among them, six were applied to establish the serpentinophyte checklist.These criteria were as follows.1, inductive: species observed on serpentine by our group since 1989 (Cabezudo & al., 1989).2, expertise: data taken from authors in the specialized literature and our own data that link taxa to serpentine.3, bibliographical: individual taxa classified as serpentinophytes in the literature.4, syntaxonomic: presence or absence of serpentinophytes in relevés and in syntaxa detected by others, such as Staehelino-Ulicion baetici, which are linked exclusively to serpentine.In addition, the 5 Fig. 2. Location and area of the peridotite outcrops in Malaga: a, Bermeja, 319 km 2 ; b, Aguas, 35 km 2 ; c, Alpujata, 71 km 2 ; d, Guadalhorce, 6 km 2 .and 6 criteria (bio-indicator and edaphic) were used to propose three types of serpentinophytes depending whether some populations of the species may grow on other substrates.
First, a bibliographical search for species cited as possible serpentinophytes was made (Rivas Goday, 1974;López González, 1975;Rivas Goday & López González, 1979;Castroviejo & al., 1986Castroviejo & al., -2011;;Blanca & al., 2011) and completed with chorological data obtained from GBIF (Global Biodiversity Information Facility in Spain) in 2011.To complete the data, a series of surveys in the peridotites of Malaga and Almeria (Fig. 1) were made (years 2009 to 2011), recording floristic (plant collecting), phenological, phytosociological (vegetation relevés), chorological (patterns of local distribution of populations) and ecological (habitat, altitude range, bioclimatic belt and rainfall range -ombrotype-Rivas Martínez, 2011) data.All the collected specimens were deposited in the University of Malaga Herbarium (MGC).Taking into account all the distributional data collected, the percentage of populations for each serpentinophyte known to grow on peridotites was estimated.This estimation was based on the number of geographically and/or ecologically separate localities for each population.Three categories of serpentinophily were described that were adapted from other categories used for plants living on soils such as dolomite and gypsum (Jeffrey, 1987;Mota & al., 2008Mota & al., , 2011) ) and depended on the ecological and chorological affinity for peridotite and serpentine substrata.1, obligate serpentinophytes: taxa linked exclusively to peridotite.2, preferential serpentinophytes: at least 90% of populations linked to peridotites.3, subserpentinophytes: at least 66% of populations linked to peridotites.We also considered some other species with a number of populations growing on peridotite, which may be regarded as subserpentinophytes following more exhaustive studies.

Other important species
Digitalis obscura L. subsp.laciniata (Lindl.)Maire grows mainly on peridotites and secondarily on dolomites and sandstones in Andalusia and Morocco.Elaeoselinum asclepium (L.) Bertol.subsp.millefolium (Boiss.)García Martín and Silvestre is endemic to the south of the Iberian Peninsula, where it mainly inhabits peridotites, although it can also be found on sandstones and dolomites.Both taxa nearly reach the limit percentage for serpentine populations to be considered as subserpentinophytes.Avenula gervaisii Holub subsp.gervaisii and Scorzonera baetica (Boiss.)Boiss.have approximately 50% of the populations growing on serpentines.

DISCUSSION
Except for Asplenium adiantum-nigrum var.corunnense and Notholaena marantae, the south Iberian serpentinophytes are considered as Mediterranean floristic elements (Blanca & al., 2011), showing eco-morphological and functional adaptations to the characteristic dry period of the Mediterranean climate (Orshan, 1986).Xeromorphic adaptations and a predominantly spring flowering season (Pérez Latorre & Cabezudo, 2002) are regarded as relevant factors for colonizing Mediterranean peridotites (Chiarucci, 2003).One exception worthy of note is Peucedanum officinale subsp.brachyradium with its autumn-flowering.
The chorological spectrum of south Iberian serpentinophytes reflects their affinity for the peridotite outcrops of Malaga province, grouped in the Bermejense phytogeograhical sector (Nieto & al., 1991).Most of the obligate serpentinophytes (20) are local endemisms except for Asplenium adiantum-nigrum var.corunnense and Notholaena maranthae, which have a wider distribution.The endemicity rate for obligate serpentinophytes is 91%.The two preferential serpentinophytes (Galium boissieranum and G. viridiflorum) are also restricted endemisms from Malaga, Cádiz and Granada provinces.Two of the subserpentinophytes (Arenaria retusa and Senecio eriopus) are restricted endemisms of Malaga and Cádiz (Senecio is also present in Granada), as is Genista hirsuta subsp.lanuginosa but this taxon reaches Morocco.74% of the serpentinophytes are local endemisms and this percentage reaches 89% if an area centered in Malaga province and surroundings is considered.
As was found with Italian peridotite outcrops (Selvi, 2007), the number of obligate serpentinophytes in Andalusia increases with the outcrop area (Table 1).Serpentinophyte richness (Fig. 3) increases with that of the log-correlated area of the outcrops (lineal adjust R 2 = 0.9087).Sierra Bermeja shows the highest richness (3.64) and is the only outcrop where all the serpentinophytes, except Centaurea carratracensis, are found.This mountain range enjoys a high protection status at both regional (Natural Site) and European (LIC) levels.Guadalhorce is the smallest outcrop and shows the lowest richness (1.54).
In contrast, the taxonomic spectrum for obligate serpentinophytes (Table 3) and dolomitophytes (Mota & al., 2008) show several differences.Fabaceae and Scrophulariaceae, both absent from the group of obligate serpentinophytes, are the best represented families amongst dolomitophytes, whereas members of Brassicaceae, Caryophyllaceae and Lamiaceae are frequent in both edaphic types.The family Asteraceae has the highest number of serpentinophyte species.Worthy note is the lack of serpentinophytes among the family Poaceae, as also occurs in eastern Greek peridotites (Trigas & Iatrou, 2006) but not in north Italian outcrops (Selvi, 2007).
When comparing Iberian serpentine endemics with other ultramafic Mediterranean areas in the world such as California (Kruckeberg, 1992;Safford & al., 2005), of particular note are the dominance of Brassicaceae and Liliaceae in Cali -South-Iberian serpentinophytes fornia (Asteraceae in the Iberian Peninsula), the presence of Galium and Allium as common serpentinophyte genera, the very few endemics among the Poaceae (none in the Iberian Peninsula), and the coincidence of bodenvag forest genera (Pinus jeffrey and Quercus vaccinifolia in California and Pinus pinaster and Quercus coccifera in the Iberian Peninsula).
The habitats and plant communities preferred by the serpentinophytes are shrublands on poorly developed soils (Staehelino-Ulicion baetici alliance in Cisto-Lavanduletea class) and the communities living on slopes, lithosols and rock fissures (alliance Andryalo-Crambion filiformis, class Phagnalo-Rumicetea indurati) (Table 4).These types of communities are the ones with the highest endemicity rate among Mediterranean habitats (Snoguerup, 1971;Gómez-Campo, 1985;Médail & Verlaque, 1997).However, one species, Galium viridiflorum stands out because it is the only serpentinophyte associated with wet ecosystems.This pattern is also found in serpentinicolous vegetation of northern Portugal and south Iberia, which shows similar trends, both being abundant in shrublands and rupicolous plant communities (Menezes & Pinto da Silva, 1992).
According to the Spanish Red List of endangered species (Moreno, 2008), the percentage of obligate serpentinophytes threatened is 59% (13 taxa), of which 45% (10 taxa) are included in the two high risk categories (CR and EN) and 15% (3 taxa) are classified as VU.If we consider all the serpentinophytes (27 taxa), 56% are threatened (15 taxa).A study carried out in northern Italian peridotites revealed that among 11 obligate serpentinophytes only one is considered as EN at a regional level (Selvi, 2007).
It is clear that adaptation to serpentine substrate is one of the main sources od endemicity, and therefore of plant diversity.Due to the exceptional nature of the vegetation and flora that are therein, which is underlined by the results of this work, the biggest of the Andalusian peridotite outcrops (Sierra Bermeja) has been proposed as National Park, the maximum protection category for natural spaces in Spain.These areas are the same as those proposed by Médail & Diadema (2009) as a phylogeographical refuge and a "hot-spot" in the context of the Mediterranean Basin (5.Serrania de Ronda), and overlap an important area for threatened Spanish flora (Bañares & al., 2003).

Table 3 .
Number and percentage of serpentinophytes indexed by families.