Taxonomic assessments and research are often underemphasized in conservation programmes and consequently some threatened species may escape attention. However, plant taxonomic and herbarium research can help conservation practitioners take appropriate action (Krupnick et al., Reference Krupnick, Kress and Wagner2009; Saad et al., Reference Saad, Talhouk and Máhy2009). The recent rediscovery of Aquilegia paui (Ranunculaceae) in north-east Spain shows how much taxonomic research is still needed even in a country with a well-known flora (Bolòs & Vigo, Reference Bolòs, Vigo and Barcino1984; Castroviejo, Reference Castroviejo1986–2010). The example of this species is representative of other restricted range plant species of isolated, impacted areas of Europe.
The genus Aquilegia L. includes nearly 70 species of perennial herbs distributed throughout temperate regions of the Northern Hemisphere. A. paui was described by Font Quer (Reference Font Quer1920) from plants collected in the Ports de Tortosa mountain range of Tarragona Province, Catalonia, Spain. Cullen & Heywood (Reference Cullen, Heywood, Tutin, Heywood, Burges, Valentine, Walters and Webb1968) recognized the species but Bolòs & Vigo (Reference Bolòs, Vigo and Barcino1984) and Díaz González (Reference Díaz González, Castroviejo, Laínz, López González, Montserrat, Muñoz Garmendia, Paiva and Villar1986) treated A. paui as a synonym or subspecies of A. vulgaris L. However, Aymerich & Sáez (Reference Aymerich and Sáez2001) and Sáez & Guàrdia (Reference Sáez, Guàrdia, Bañares, Blanca, Güemes, Moreno and Ortiz2003) later tentatively accepted A. paui and assessed it as Critically Endangered (IUCN, 2001) because of its narrow geographical distribution and low number of reproductive individuals. Finally, after the discovery of original herbarium type material, Martinell et al. (Reference Martinell, Sáez and Molero2007) demonstrated that the taxonomic debate arose from a mistake, when mixed specimens of A. paui and A. vulgaris, both occurring in the same area in Els Ports massif, were included in Font Quer’s exsiccata Flora Iberica Selecta. They concluded that A. paui (Plate 1) is a distinct, well-defined species restricted to a limited area.
Plate 1 Aquilegia paui Font Quer growing in the Montcaro area of the Els Ports Massif. Photo: L. Sáez.
Recent fieldwork resulted in the rediscovery of the single known population of A. paui, enabling us, after comparisons with herbarium specimens, to confirm the specific status of this extremely narrow endemic and to assess its conservation status. We conducted 20 surveys in Els Ports massif during 1999–2008, visiting all localities in which A. paui had been reported by previous authors, and other areas in this mountain range potentially suitable for this species. We surveyed a total of 31 1-km2 UTM squares but found A. paui in only two, in the Montcaro area, the highest summit of the Els Ports massif, where the species was originally found by Font Quer (Fig. 1). It grows in a narrow altitudinal zone (990–1,390 m) on calcareous shady cliffs and scree, mainly with northern exposures. Populations in other localities reported for A. paui contained only A. vulgaris.
Fig.1 Location of the four subpopulations (AP1–4) of Aquilegia paui in the Montcaro area. Dark lines are roads and contour lines are at 100 m intervals; coordinates are UTM (European Datum 1950, Zone 31T). The black rectangle on the inset indicates the location of the main figure in north-east Spain.
We counted all reproductive and vegetative individuals. As two non-adjacent rosettes may come from a common underground stem, thus obscuring the difference between ramets and genets, we considered as different entities those rosettes that were separated by more than 20 cm. We identified four subpopulations (Table 1). The distribution of the species is very restricted, with an extremely low area of occupancy (0.12 km2; the area within the extent of occurrence, EOO, that is occupied by a taxon, where EOO is the area contained within the shortest continuous imaginary boundary that can be drawn to encompass all the known sites of occurrence of a taxon, excluding cases of vagrancy; IUCN, 2001) and extent of occurrence (0.60 km2). A decline in the population is inferred by the quality of the habitat, and we also recorded fluctuations in the number of mature individuals. We therefore recommend that A. paui is categorized as Endangered based on the criteria (IUCN, 2001) B1ab (iii) c (iv) +B2 ab (iii) c (iv).
Table 1 For the populations AP1–3 of Aquilegia paui (Fig. 1, Plate 1) the area of occupancy (AOO) and number of mature individuals (and in parentheses the number of reproductive individuals achieving fruit ripening, excluding aborted flowers and predated fruits) located during surveys in 2005–2008. Surveys of subpopulation AP4 (Fig. 1), discovered in 2008, are ongoing.
The vulnerability of this species is high, with extremely low levels of genetic diversity and low recruitment rates (Blanché et al., Reference Blanché, Molero, Rovira, Simon, Bosch and Sàez2005). A. paui appears to reproduce well by rhizomes (not by seed) in situ although it is not easily cultivated ex situ. The conservation of the endemic wild goat Capra pyrenaica subsp. hispanica, which may be overgrazing subpopulations AP2 and AP3, in Parc Natural dels Ports may be in conflict with the conservation of A. paui, as in other mountain areas in which plant conservation programmes and hunting reserves coexist (Simon et al., Reference Simon, Bosch, Molero and Blanché2001).
The impact of human activities on A. paui does not currently appear to be particularly significant, although two subpopulations are located next to a road and may be affected by climbers and trekkers. Rock-climbing is increasingly popular on the cliffs at Montcaro and plant cover is reduced near the base of climbing routes, where A. paui grows. Recent regulations issued by Parc Natural dels Ports authorities prohibit this activity where A. paui occurs.
The summit of Montcaro has been severely altered by the construction of telecommunications facilities, including an access road, and the peak is frequented by visitors and maintenance staff. Such disturbances may have affected one subpopulation of A. paui, which experienced a reduction in the number of individuals and area of occupancy during 1999–2007 (J.C. Baiges & L. Sàez, unpubl. data), mainly because of the deposition of waste in the construction of the telecommunications devices. A further potential threat is forest fires. A fire in north-west Parc Natural dels Ports in July 2009, near the village of Horta de Sant Joan, destroyed 1,000 ha and killed five firemen. This area, < 10 km from the populations of A. paui, had already been burnt 20 years earlier.
The conservation of A. paui is an example of the difficulties of designing appropriate conservation strategies for such species in the Mediterranean and, particularly, the Iberian Peninsula, where there are many threatened plant taxa (Moreno, Reference Moreno2008) and a high percentage of endemics, many extremely restricted (Bañares et al., Reference Bañares, Blanca, Güemes, Moreno and Ortiz2003). Management of narrow endemic plant species in Spain has mostly been addressed with recovery plans for individual species. However, the available resources and the pace at which these legal instruments and their implementation function are too slow to halt the loss of populations.
It is not uncommon for extremely narrow endemics to exist in only 1–5 subpopulations, as with A. paui. There are five conservation steps that can be considered for such species, described here in increasing order of complexity and cost.
Habitat protection Passive habitat protection is not a guarantee of long-term conservation. Some of the now extinct species that formerly survived in only 1–2 known populations (e.g. Kunkelliella psitoclada, Normania nava and Aeonium mascaense in the Canary Islands; Thymus funkii in southern Spain) were lost despite growing in areas with some protection (Bañares et al., Reference Bañares, Blanca, Güemes, Moreno and Ortiz2003). Reinforced habitat protection is required. An example is the small and actively managed area in Magalluf (Balearic Islands) where several point endemic Limonium species are conserved by a multi-species recovery plan focused on a few square metres in an urban area (Govern de les Illes Balears, 2009).
Diversification of risk Occurrence in only 1–2 subpopulations, even if there are no immediate threats and plants seem well adapted to estenoic (i.e. very narrow range) ecological conditions (such as rocky places, as for many Mediterranean narrow endemics; cf. Lavergne et al., Reference Lavergne, Thompson, Garnier and Debussche2004), will not counteract stochastic events. Establishment in at least a third site and ex situ measures are required. In Spain, in addition to Protection zones under EU law (Sites of Community Importance, SCI), each Autonomous Government developed a variety of legal measures to protect such small sites (so-called Microreserves, Espais d’Interès Natural or Reserves Naturals). A realistic objective, although it depends on the biology of each species, is to maintain a minimum viable population greater than the cut-off point for the Endangered category (250 individuals; IUCN, 2001) for each of a minimum of three subpopulations. The minimum size of such small reserves needs to be carefully planned (Albert et al., Reference Albert, Escudero and Iriondo2001; Colas et al., Reference Colas, Olivieri and Riba2001).
Field research Although there is good floristic knowledge for some of the Mediterranean countries, intensive plant surveys are required in remote and/or unexplored locations to facilitate the location of currently unknown subpopulations of narrow endemic plant species. The relocation of A. paui is an example of the value of such surveys.
Monitoring Monitoring, including population viability analysis, population genetics and reproductive biology, can be used to adapt long-term conservation strategies for individual species. For long-lived, demographically stable species creation of additional new populations close to the original can be effective (e.g. Borderea chouardii in the Pyrenees; García et al., Reference García, Goñi, Guzmán, Iriondo, Cosculluela and Puente2007). However, for demographically unstable species or those undergoing severe declines (e.g. annuals or short-lived monocarpic species such as Seseli farrenyi on the Mediterranean coast; López-Pujol et al., Reference López-Pujol, Martinell, Massó, Blanché and Molero2010), both in situ (reinforcement, reintroduction, establishment of new populations) and ex situ (germplasm preservation, propagation techniques) measures may be required.
Reintroduction For non-viable natural populations or species extinct in the wild reintroduction may be the only option but requires careful consideration. The attempts to reintroduce Lysimachia minoricensis to its natural habitat in Minorca failed because of lack of knowledge of the species’ ecological requirements and the low genetic diversity of the ex situ population (Ibáñez et al., Reference Ibáñez, Calero, Mayol and Rosselló1999). Efforts to establish new populations of the extremely narrow endemic Diplotaxis siettiana on Alboran Island, southern Spain, managed, at the third attempt, to establish a population of 50 individuals (Mota, Reference Mota2003), which is at the threshold for a minimum viable population. As the probability of success in such cases is low, such reintroduction can probably only be justified if sufficient new knowledge will be obtained to help future reintroductions (Colas et al., Reference Colas, Olivieri and Riba2001; Krauss et al., Reference Krauss, Dixon and Dixon2002).
In the case of A. paui, in accordance with these five steps, we propose the following conservation measures: (1) monitoring and surveys, as well as additional field exploration in suitable sites, in Parc Natural dels Ports; (2) preventive management (limiting overgrazing and climbing activities); (3) research on population genetics and demography, and seed germination and multiplication techniques, and to evaluate the results after 3 years and then prepare a long-term recovery plan if necessary.
If the distinctiveness of A. paui had not been assessed it would have remained unidentified, immersed amongst the forms of the widely distributed, non-threatened A. vulgaris. However, A. paui was identified in time to be included in a new list of the protected plants of Catalonia (DOGC, 2008). The case of this species is an example of the plight of other potentially neglected rare species that are facing extinction in anonymity because their taxonomic status has been misunderstood or overlooked.
Acknowledgements
We thank two anonymous referees for their helpful comments, and JC. Baiges, S. Massó, M. Bosch, J. Mestre, A. Buira and the staff of Parc Natural dels Ports for help in the field. This research was supported by Grants CGL2007-60475/BOS, FBG Agreement (DMAH, Generalitat de Catalunya) and a Research Fellowship (Universitat de Barcelona) to MCM.
Biographical sketches
The authors belong to a research group (GReB, http://www.greb.org.es/joomla/) with more than 20 years of interest in the systematics and conservation of Mediterranean flora. The group’s current projects are devoted to the systematics of Campanulaceae, Ranunculaceae and Compositae, to conservation biology, including demography, reproduction, pollination biology and population genetics of narrow endemics, and to studies of the origin of the endemic flora of the Mediterranean, Asia and South America.
