The reintroduction of plants (the controlled placement of plant material into a natural or managed area; Godefroid et al., Reference Godefroid, Piazza, Rossi, Buord, Stevens and Aguraiuja2011) is a relatively recent development and a potentially important tool for conservation. The rationale for reintroduction is the establishment of new or augmentation of existing populations to increase the survival prospects of a species (Pavlik, Reference Pavlik, Falk, Millar and Olwell1996). IUCN (1998) encourages reintroduction as a strategy to prevent the extinction of plant species. The potential of reintroduction to contribute to the recovery of threatened species is significant, and is enhanced when part of integrated conservation activities (Albrecht et al., Reference Albrecht, Guerrant, Maschinsky and Kennedy2011).
Dianthus L. (Caryophyllaceae) is one of the most differentiated plant genera in Europe, characterized by several endemic taxa in the Mediterranean area (Valente et al., Reference Valente, Savolainen and Vargas2010). In Sardinia eight endemic species of Dianthus have been recorded (Bacchetta et al., Reference Bacchetta, Brullo, Casti and Giusso del Galdo2010), four of which are narrowly distributed; among these, Dianthus morisianus Vals., the only psammophilous species of the genus in the Mediterranean basin and with only one population, on the Portixeddu coastal dune system in Buggerru, south-west Sardinia (Fig. 1), is one of the most threatened plants on the island (Bacchetta et al., Reference Bacchetta, Fenu and Mattana2012).
D. morisianus is a perennial herb characterized by numerous woody stocks, erect stems and a basal rosette with thin and linear leaves. The stems bear terminal multi-flowered heads; the calyx is characterized by lanceolate teeth and the colour of the corolla is pink. The flowering season is from early May to late June, and ripe fruits can be found during June–July (Bacchetta et al., Reference Bacchetta, Brullo, Casti and Giusso del Galdo2010). This plant grows on stabilized dunes at the edge of Juniperus spp. micro-forests and scrub dominated by Cistus spp.
The natural habitat of D. morisianus has been strongly modified by human activities, causing habitat loss and fragmentation: there are several settlements in the species’ habitat and since 1950 much of the dune system has been afforested to stabilize the dunes and halt the movement of sand inland. The small size of the population and the limited seedling recruitment make D. morisianus potentially prone to extinction, and it is categorized as Critically Endangered on the European (Bilz et al., Reference Bilz, Kell, Maxted and Lansdown2011) and Global Red Lists (Fenu et al., Reference Fenu, Mattana and Bacchetta2011). The Autonomous Region of Sardinia funded a conservation project for D. morisianus because it is one of the most threatened plant on the island (Bacchetta et al., Reference Bacchetta, Fenu and Mattana2012). The project comprises in situ and ex situ research and experimental projects, such as the construction of protective fences (Fenu et al., Reference Fenu, Mattana and Bacchetta2012) and the reintroduction described here.
Detailed knowledge of a species’ ecology and reproductive biology is required prior to reintroduction (IUCN, 1998). Preliminary research focused on the ecology of D. morisianus and the level of human disturbance in its habitat. These surveys facilitated the identification of a suitable area c. 150 m from the natural population (Fig. 1), in a protected site, managed by public administration (EFS, Ente Foreste della Sardegna); conservation of threatened plants is more practicable on legally protected than on private land (e.g. Ali & Qaiser, Reference Ali and Qaiser2011). The chosen site was most likely a part of the species’ former range and had not been greatly altered by human activities.
Reintroduction success is greater when using material originating from multiple populations (Vergeer et al., Reference Vergeer, van den Berg, Roelofs and Ouborg2005) but this is not possible when working with a narrowly distributed species. Seedlings germinated from seeds collected in different years were therefore used to facilitate the inclusion of some genetic diversity. Fruits were collected from the wild population in 2008 and 2009, by sampling 50 mature plants in each year. Seedling emergence and establishment are the most critical stages in the life cycle of D. morisianus (Cogoni et al., Reference Cogoni, Mattana, Fenu and Bacchetta2012) and therefore juvenile plants were used for the reintroduction. In a laboratory 200 seeds (100 per collection) were sown and incubated at the optimal germination temperature (15 °C; Cogoni et al., Reference Cogoni, Mattana, Fenu and Bacchetta2012). Subsequently, all the seedlings (92 and 94 for the first and second sowing, respectively) were placed in pots with sand collected in the species’ habitat. Successful growth requires adaptation to environmental conditions and thus propagation requires hardening, to decrease the stress of planting out and increase survival (Aguraiuja, Reference Aguraiuja2011); accordingly, no horticultural treatments were adopted. In November 2010 the 113 surviving plants (50 and 63 from the first and the second sowing, respectively) were reintroduced to the chosen site. The plants were placed in nine groups at a mean distance of c. 15 m from each other (Plate 1); the location of each group was determined by the availability of suitable microhabitats. The plants were then monitored monthly.
A key measure of the success of a plant reintroduction is the survival rate, the transplants ability to flower and set fruit, and the recruitment of new individuals (IUCN, 1998; Menges, Reference Menges2008; Godefroid et al., Reference Godefroid, Piazza, Rossi, Buord, Stevens and Aguraiuja2011). The survival rate was high, with few plants dead in the first year and those remaining were alive after 24 months (Table 1). Forty and 65% of the plants became reproductive in the first and second years, respectively. The mean number of fruits per plant was 3.84 ± SE 2.48 and 7.97 ± SE 7.11 in the first and second years, respectively (Table 1), higher than that in the natural population (2.60; D. Cogoni et al., unpubl. data). The number of seedlings produced by the reintroduced plants (87; Table 1) is higher than recorded in the natural population, where seedlings comprise 9.95% of the population (D. Cogoni et al., unpubl. data). This is an important indicator for measuring reintroduction success, because recruitment is severely limited by summer drought in Mediterranean type ecosystems (Herrera, Reference Herrera1992).
As far as we are aware there have been few reintroductions of plants on coastal dune systems in the Mediterranean Basin. Survival to the first summer is a key factor for measuring the success of a plant reintroduction (Ballesteros et al., Reference Ballesteros, Cañadas, Foronda, Fernández-Ondoño, Peñas and Lorite2012) and on this measure the reintroduction of D. morisianus has been effective. In this habitat a reintroduction in autumn allows the plants to stabilize before the summer drought, and using an appropriate microhabitat, something unique to each taxa, is a key feature for successful plant reintroduction (Menges, Reference Menges2008; Reckinger et al., Reference Reckinger, Colling and Matthies2010). If a suitable microhabitat can be located management activities such as watering may not be needed in the early stages of a reintroduction (Aguraiuja, Reference Aguraiuja2011).
There is a positive relationship between the number of reintroduced plants and their survival, and using larger plants generally improves the success of reintroductions and reduces the mortality rate (Reckinger et al., Reference Reckinger, Colling and Matthies2010; Godefroid et al., Reference Godefroid, Piazza, Rossi, Buord, Stevens and Aguraiuja2011). Demographic and genetic theories both predict that the persistence time of a population increases with its initial size (Robert et al., Reference Robert, Couvet and Sarrazin2007), and the effects of demographic stochasticity is lower in populations with > 50 plants (Menges, Reference Menges1991). Knowledge of the biology of a species, in particular the critical life-cycle stage for survival, is crucial for reintroduction planning (Maunder et al., Reference Maunder, Havens, Guerrant, Falk, Guerrant, Havens and Maunder2004), and expertise in ex situ multiplication and cultivation procedures, for emulating natural conditions, is a prerequisite (Aguraiuja, Reference Aguraiuja2011). All considered, reintroduction is generally a relatively high-risk, high-cost activity (Gorbunov et al., Reference Gorbunov, Dzybov, Kuzmin and Smirnov2008). The reintroduction of D. morisianus, however, is an example of a low-cost project: the involvement of researchers, public authorities and local stakeholders was voluntary, and site management was not intensive. Although at this stage the project is positive for all proposed indicators (Menges, Reference Menges2008; Godefroid et al., Reference Godefroid, Piazza, Rossi, Buord, Stevens and Aguraiuja2011) long-term monitoring is planned, to examine the ecological and economic viability of the restoration options adopted. We believe that this reintroduction project can serve as a model for the reintroduction of other threatened species of the coastal dunes of Sardinia and, more widely, of the Mediterranean area.
Acknowledgements
This research was supported by the Assessorato Difesa Ambiente and EFS (Regione Autonoma della Sardegna). The authors thank Mario Angioy and colleagues of EFS for their help with the fieldwork.
Biographical sketches
Donatella Cogoni, Giuseppe Fenu and Erica Concas have a particular interest in conservation of the threatened endemic plants of Sardinia. Gianluigi Bacchetta carries out geobotanical analyses in the western Mediterranean. The group's research is focused on conservation biology, including the demography, reproductive and pollination biology and population genetics of narrow endemic plant species.