Breeding system and ecological traits of the critically endangered endemic plant Limonium barceloi (Gil and Llorens) (Plumbaginaceae) Zeeba Khan1, Gabriel Santpere2 and Anna Traveset1

Phone #: +34 971 611718

Fax #: +34 971 611761

ABSTRACT
Limonium barceloi (Plumbaginaceae) is a narrow endemic seasonal halophytic plant, uniquely found in a highly degraded urban wetland in the Bay of Palma Mallorca, located in the northwest Mediterranean. It was awarded critically endangered status in 2004 and is the subject of a recovery plan administered by local government. Despite this, the last ten years have seen a dramatic decline in the population from c. 3000 individuals to just c. 300; reasons for this decline are principally anthropogenic disturbance. Here we present the results of an investigation into some aspects of the reproductive biology of this species in the last remaining in situ population, in order to gain insight into its limited distribution and abundance, and to guide further development of management strategies. Findings indicate that although it provides important floral resources to a number of insect visitors, the plant is an autonomous apomictic that may also be functioning as an obligate asexual reproducer and low genetic variation is suspected.. Germinability is observed to be at c. 70% and was positively correlated with maternal plant size characteristics. Two seed predators, the moth Goniodoma limoniella (Coleophoridae) and the ant Messor bouvieri (Myrmicinae) were discovered affecting both pre- and post-dispersal seeds. Rate of removal was high, although it is hypothesised that at this time species recruitment is not seed limited, but rather restricted by lack of suitable microsites. The results of this study are used to make recommendations for the species recovery.

Keywords: apomixis, Balearic Islands, plant conservation, plant recovery plans, reproductive biology, sea lavender.

1. Introduction
Recovery plans for endangered plants often require the creation of new, self-sustaining populations within their historic range and habitat (Knudsen, 1987; Whitten, 1990; Pavlik et al., 1993). Unfortunately, creating new self sustaining populations that possess the genetic and ecological characteristics of natural populations remains a great challenge (Pavlik et al., 1993; Heywood and Iriondo, 2003) and ought to begin with experiments to determine the ecological factors governing the growth of the founding population (Schemske et al., 1994). Amongst the key questions to be addressed are: what factors determine the viability of the population?, which life stage is most critical for the viability of the population?, and which management strategy offers the greatest chances for facilitating the survival of the population? (Schemske et al., 1994; Heywood and Iriondo, 2003).

To provide adequate answers to these questions, a systematic collection of baseline data on the natural history of the species is needed (Schemske et al., 1994). A set of actions can then be established to minimise these factors, to reverse the declining trends and to fulfil the objectives of the recovery plan (Heywood and Iriondo, 2003).

The Spanish Balearic Islands, part of the Tyrrhenian islands (Sicily, Sardinia, Corsica, Balearic Islands) located in the North-western Mediterranean, is a “hotspot within a hotspot” for plant biodiversity (Medail and Quézel, 1999) and currently eleven endangered plants are the subject of recovery plans. Ten of these species plans have as an objective the creation of new populations within the historic range (Conselleria de Medi Ambient, 2007). One of the most emblematic of all the threatened Balearic plant species is the critically endangered endemic Limonium barceloi (Gil and Llorens). A member of the Plumbaginaceae, this sea lavender belongs to the family with the most endangered and rare species in Spain, where approximately 75% are considered endemic (Palacios and González-Candelas, 1997).

L. barceloi, described for the first time in 1991 (Gil and Llorens, 1991), is found uniquely in a small, highly degraded wetland area of 32 hectares known as Ses Fontanelles (39º32´05.92” N/ 2º43´41.60” E), located in the Municipal district of Palma de Mallorca. L. barceloi was included first in the Balearic Catalogue of threatened plants in 2001 (Sáez and Rosselló, 2001) and later was incorporated into the IUCN Red List as critically endangered (Rosselló and Sáez, 2004). It is considered emblematic, as due to its presence in the remnant wetland, the last remaining habitat of its kind in the Bay of Palma (Amengual and Ramis, 2002) it is perceived to be a flagship species for the site.
Since it was first described, the plant’s distribution has reduced dramatically. Comparable with many other Mediterranean endemics with highly restricted ranges, the principal threats come from habitat destruction and fragmentation, as land is converted to accommodate tourist resort developments and the associated infrastructure (Blondel and Aronson, 1999). A census conducted by the Sóller Botanical Garden in 2000 revealed approximately 3000 plants in Ses Fontanelles divided into 3 subpopulations (JBS Report, 2001). In 2009, a second census revealed that just 301 individuals remain (Khan and Traveset, 2009a). This dramatic reduction of 90% of the population in less than 10 years is the result of anthropogenic based disturbances, namely construction activities on site during the building of an aquarium, and later the accidental flooding of the site with fresh water (Khan and Traveset, 2009a). The current in situ population of L. barceloi is divided between a subpopulation of 297 and another of 4, that for the purposes of this study are named hereafter A and B, respectively.

A recovery plan for this species was initiated in 2007 by local government. Amongst the objectives was the creation of a study site for propagation and research. Plants are grown from seed taken from the wild population, with the aim of reintroduction to the site so that the species might reoccupy its former distribution (Vicens and Bibiloni, 2007).

Seeds extracted were placed in 85mm Petri dishes on top of a disc of filter paper and submerged in 8ml of distilled water and placed in a germination chamber at 18º C with a 12 hour photoperiod. These conditions were chosen as the optimum germination characteristics for the species based on earlier studies carried out by Bibiloni (2000). The number of seeds that germinated after one week was recorded. Germination was considered to have occurred on emergence of radicle.

Data were collected for each of the 30 plants from which inflorescences were collected. This included height, diameter, number of stems, and number of flowers. Seeds were extracted for 20 of the samples and placed in Petri dishes in optimum conditions for germination (Bibiloni, 2000). Germination was considered to have occurred on emergence of the radicle.

When examining seeds from the different treatments, we noticed that a fraction of them were predated by insect (moth) larvae. We thus recorded the number of preyed seeds and seed set was based on actual seed count plus evidence of seed presence via moth predation holes.
2.5. Seed predation studies
Preliminary studies revealed the presence of two seed predators: a moth affecting pre-dispersal of seeds and an ant predating on pre- and post-dispersed seeds. Individuals were collected and sent for identification. We wanted to assess the impact of seed predation by moths and ants. For moths, we randomly chose 100 calyces from 20 of the samples taken from the plants (those used to establish seed set), and these were examined for evidence of seed predation by the moth. The presence of small holes at the base of the calyx was considered to be sign of moth predation and a seed count was also taken for the same samples. Observations were also made of ant predation of L. barceloi seeds at the A and B populations. Both pre- dispersal predation and post-dispersal predation was observed. Four counts of 10 minutes were made on three different dates (25^th September, 13^th October, 27^th October) to measure the rate of pre-dispersal seed removal by ants on plants from the A population. Seeds were included in the count when they were removed from the plant. Whether the seeds arrived at the nest, or were lost along the way was not considered. On three dates in 2010, 12^th August, 25^th August, 9^th September, post-dispersal seed predation was assessed. Four piles of 300 seeds were placed at random locations around the base of the plants in the subpopulation A on each of the three dates. After a period of 24 hours, seeds were collected and recounted. Material discarded from ant nests was also collected from middens located adjacent to two of the entrance sites situated next to the subpopulation of L. barceloi on each of the following dates 25^th August 2009, 3^rd September 2009, 12^th August 2010 and 18^th November 2010. Three samples of 4 g were taken and divided into L. barceloi plant matter and other plant matter. The different sets of material were then weighed to the nearest 0.0001mg with a Denver TARE balance.
2.6. Data analyses

Seed set in the two treatments and the control for the pollination experiments were compared by means of an ANOVA, after normalising the proportions with the angular transformation. Predation data was subjected to basis descriptive analysis and a general linear model was constructed to predict seed germinability, using number of flowers produced and number of predated seeds (bearing larval exit holes) as main effects. The R-system of statistical computing (R Development Core Team 2009) was employed for all analyses.

The tetraploid nature of L. barceloi suggests diplospory as the probable mechanism for asexual production of seeds, as there exists a strong correlation with tetraploidy and diplospory (Asker and Jerling, 1992). Whitton et al. (2008) suggest that individuals exhibiting diplospory are also more likely to be obligate asexual reproducers and while the existence of obligate apomictic species is controversial (Koltunow and Grossniklaus, 2003; Tucker et al., 2003), evidence suggests that L. barceloi may currently be functioning as obligate apomictic. High numbers of morphological anomalies are observed in the pollen (Bibiloni, 2000). This is a characteristic of a high frequency apomixis mediated reproduction (Maynard Smith, 1978; Eckert, 2002) and the presence of one of the study plants that produced flowers and no seeds could be an expression of the deleterious mutational load common in asexually reproducing plants as described by Navascués et al. (2010). Navascués et al. (2010) assert that this feature may develop under specific conditions such as self incompatibility, low population size and high clonal rate. Genetic testing would be required to confirm or refute this hypothesis and more research in this area is suggested.

Results on seed predation studies revealed two predators working at different phases in the plant’s life cycle. Moths affect pre-dispersal and ants the pre- and post- dispersal. Gonoidoma limoniella (Coleophoridae) was first described for Spain in 1996 (Vives Moreno, 1996). It is a pre-dispersal moth seed predator common to the Limonium genus. A high level of variation in predation rates, which can reach up to 78% of the seeds was found, but these rates were not correlated to plant size. The genus Messor is an important group of granivorous ants in Mediterranean systems (Diaz, 1994; Detrain and Tasse, 2000; Azcárate and Peco, 2007) and we found that Messor bouvieri (Myrmicinae) is an important predator of the L. barceloi seeds, indicated by both the removal rate (8.68% of seeds available in 24 hours) and a high percentage of L. barceloi material found in middens (41.33%). Granivorous ants are commonly known to influence population dynamics of plant species through selective predation and dispersal (Janzen, 1971; Andersen, 1989; Brown and Human, 1997; Retana et al., 2004); however, their effect on perennial plant populations is at present incompletely understood. Further, while our study examined rates of removal from plants and from controlled seed additions, no assessment was made of seed loss or abandonment en route to the nest; thus, we cannot discard the possibility that ants play a role in dispersal, favouring seedling establishment into new microsites.

In assessing the impact of seed predators, it would be wrong to assume that seed removal rates are equal to predation (Retana et al., 2004; Vander Wall et al., 2005; Martínez-Duro et al., 2010) and very few studies have looked at the effect of seed predators on recruitment rates in endangered, rare plants. Those that have been completed have found different results. Albert et al. (2005) showed that seed predation, although high, did not limit population growth for the rare Erodium paularense in central Spain, while White and Robertson (2009) discovered the contrary for Lepidium papilliferum, a rare perennial herb in the US. It is thought probable that due to the high seed bank that has been reported for the species (Bibiloni, 2000), recruitment in L. barceloi is not seed limited at this time, although more studies should be undertaken to assess the validity of this hypothesis.
5. Conclusions and recommendations for future conservation and management

Small populations are infamously prone to extinction from stochastic events (Goodman, 1987) and at present the habitat of L. barceloi enjoys no official protected status and is under constant threat of urban development. Therefore, a priori action should be the setting aside of subpopulation A as a micro reserve. Laguna et al (2004) found that micro reserves were a useful tool offering effective protection for endangered plants in the Mediterranean context and the size of the subpopulation (c. 300 plants) allows it fit within the criteria defined by Frankel and Soulé (1981) and Lesica and Allendorf (1991), who suggest that a population of at least fifty individuals is required to avoid loss of genetic variation within plant populations in the short term.

Suitable habitat creation could also be initiated and plants translocated from the ex situ study sites to form new populations. We do not consider feasible the creation of subpopulations away from the plant´s historic range, due to the lack of available salt marsh sites in Mallorca. The creation of new habitat and additional subpopulations within Ses Fontanelles is the only realistic hope for the species´ continued survival and additional subpopulations could provide the potential to expand the genetic base of the species.

It should be recognised also that the timing of plantings is vital, as is the use of multiple sites. Further, it is suggested that large numbers of individuals are sown (Frankham et al., 2002) and that due to the vulnerability of seeds and seedlings (Primack and Drayton, 1997) managers should consider transplanting young plants (Davy, 2002). The implementation of extended monitoring procedures of at least 10 years is recommended, to evaluate success based on long term results (Godefroid et al., 2011).

In order to effectively create suitable habitat, it is recommended that further studies into the ecological requirements of the species are undertaken; autecological studies are considered a critical pre-requisite to conservation science and action (Simberloff, 1988, Brussard, 1991; Schemske et al., 1994). Further, as it is seen that large plants produce fitter seeds, it is advised that a variety of soil substrates, soil saturation levels and salinity concentrations are experimented with in order to ascertain which provide for greater growth rates.

Finally, it is strongly recommended that a full genetic analysis of the variation in the species is undertaken; Godefroid et al. (2011) found that the rates of survival for reintroduced species were greater when an understanding of the level of genetic diversity is included in the project design.

We are especially grateful to Clara Vignolo and Gil Panades Nieto for their help in the laboratory and with statistical analysis. Magí Franquesa and Gabriel Bibiloni provided useful information and previous relevant reports. The Conselleria de Medi Ambient, especially Eva Moragues, helped with permissions and background data and we are also indebted to the taxonomists Martin Honey and Xavier Espadaler for moth and ant identification, respectively. Finally, the Consortium Playa de Palma financed the project through an IMEDEA interdisciplinary study.

Alexander, H.M. 1985. Experimental ecological genetics in Plantago. The effects of maternal temperature on seeds and seedling characteristics in Plantago lanceolata. Journal of Ecology 73 (1), 271-282.

Amengual Pons, L., Ramis Crespi, X. 2002. Anàlisi de Ses Fontanelles i del seu entorn i propostes d'actuació, planificació i gestió per tal de millorar la qualitat ambiental d'aquest espai. Universidad de las Islas Baleares. Spain.

Andersen, A. N. 1989. How important is seed predation to recruitment in stable populations of long-lived perennials? Oecologia 81 (3), 310–315.

Asker, S.E., Jerling, L. 1992. Apomixis in plants. CRC Press, Boca Raton, Florida, USA.

Azcárate, F.M., Peco, B. 2007. Harvester ants (Messor barbarus) as disturbance agents in Mediterranean grasslands. Journal of Vegetation Science 18 (1), 103–110.

Bibiloni, G. 2000. Informe del Pla de recuperació de Limonium barceloi Gil & Llorens. Segon informe. Jardi Botànic de Sóller, Mallorca, Spain.

Bibiloni, G. 2001. Informe del Pla de recuperació de Limonium barceloi Gil & Llorens. Tercer informe. Jardi Botànic de Sóller, Mallorca, Spain.

Blondel, J., Aronson, J. 1999. Biology and Wildlife of the Mediterranean region. Oxford University Press. Oxford, UK.

Brown, M.J.F., Human, K.G. 1997. Effects of harvester ants on plant species distribution and abundance in a serpentine grassland. Oecologia 112, 237–243.

Brussard, P. F. 1991. The role of ecology in biological conservation. Ecological Applications 1, 6-12.

Chasnov, J.R. 2000. Mutation-selection balance, dominance and the maintenance of sex. Genetics 156, 1419–1425.

Conselleria de Medi Ambient. 2007. Libro blanco de protección de especies. Conselleria de Medi Ambient, Govern de les Illes Balears, Spain.

Davy, A. 2002. Establishment and manipulation of plant populations and communities in terrestrial systems, in: Perrow, M.R., Davy, A.J. (Eds.), Handbook of ecological restoration. Principles of restoration vol. 1, Cambridge University Press, Cambridge, UK, pp. 223–241.

Detrain, C., Tasse, O. 2000. Seed drops and caches by the harvester ant Messor barbarus: do they contribute to seed dispersal in Mediterranean grasslands? Naturwissenschaften 87, 373–376.

Diaz, M. 1994. Spatial and temporal patterns of granivorous ant seed predation in patchy cereal crop areas of central Spain. Oecologia 91, 561–568.

Donohue, K., Schmitt, J. 1998. Maternal environmental effects in plants. Adaptive plasticity?, in: Mousseau, T.A., Fox, C.W. (Eds.), Maternal effects as adaptations. Oxford University Press, Oxford, UK, pp. 137–158.

Eckert, C.G. 2002. The loss of sex in clonal plants. Evolutionary Ecology 15, 501–520.

Erben, M. 1993. Genus Limonium Mill, in: Castroviejo, S., Aedo, C., Cirujano, S., Laínz, M., Montserrat, P., Morales, R., Muñoz Garmedia, F., Navarro, C., Paiva, J., Soriano, C. (Eds.), Flora Ibérica. Real Jardín Botánico-CSIC. Madrid, Spain, vol. 3, pp. 85.

Erben, M. 1979. Karyotype differentiation and its consequences in Mediterranean Limonium. Webbia 34 (1), 409-417.

Fenner, M. 1991. The effects of the parent environment on seed germinability. Seed Science Research 1, 75–84.

Flora Iberica. www.floraiberica.org Accessed 27.11.2011

Frankel, O., Soulé. M. 1981. Conservation and evolution. Cambridge University Press, Cambridge, UK.

Frankham, R., Ballou, J.D., Briscoe, D.A. 2002. Introduction to conservation genetics. Cambridge University Press, Cambridge, UK.

Galloway, L.F. 2001. The effects of maternal and paternal environments on seed characters in the herbaceous plant Campanula americana (Campanulaceae). American Journal of Botany 88, 832–840.

Gil, Ll., Llorens, Ll. 1991. Limonium barceloi y L. bolosii (Gil i Llorens), nuevas especies de la isla de Mallorca (Baleares). Anales del Jardín Botánico de Madrid 49 (1), 51-56.

Godefroid, S., Piazza, C., Rossi, G., Buord, S., Stevens, A.D., Aguraiuja, R., Cowell, C., Weekley, C.W., Vogg, G., Iriondo, J.M., Johnson^, I., Dixon, B., Gordon, D., Magnanon, S., Valentin^, B., Bjureke, K., Koopman, R. Vicens, M., Virevaire, M., Vanderborght, T. 2011. How successful are plant species reintroductions? Biological Conservation 144 (2), 672-682.   

Goodman, D. 1987. The demography of chance extinction. In: Soulé, M.E. (Eds.), Viable populations for conservation. Cambridge University Press, Cambridge, UK, pp. 11-34.

Heywood, V.H., Iriondo, J.M. 2003. Plant conservation: old problems, new perspectives. Biological Conservation 113, 321–335.

Hörandl, E. 2008. Evolutionary implications of self-compatibility and reproductive fitness in the apomictic Ranunculus auricomus polyploid complex (Ranunculaceae). International Journal of Plant Sciences 169 (9), 1219 -1228.

Izmailow, R.1996. Reproductive strategy in the Ranunculus auricomus complex (Ranunculaceae). Acta Societatis Botanicorum Poloniae 65, 167–170.

Janzen, D. H. 1971. Seed predation by animals. Annu. Rev. Ecol. Evol. S. 2, 465–492.

JBS (Jardí Botànic de Sóller). 2001. Pla de recuperació de Limonium barceloi Gil i Llorens. Quaderns de la natura 8. Conselleria de Medi Ambient. Govern de les Illes Balears, Spain.

Khan, Z., Traveset, A. 2009a. Informe sobre el estado actual de la población de Limonium barceloi (Gil & L. Llorens) in situ en Ses Fontanelles 2009. Unpublished report. IMEDEA UIB-CSIC. Mallorca, Spain.

Khan, Z., Traveset, A. 2009b. La biodiversidad terrestre, in: Morales-Nin, B., Iglesias, A. (Eds.), La adaptación al cambio climatico y la preservación de ecosistemas naturales, terrestres y marinos en el marco del proyecto estrategico de recualificaión integral. Documento 2. Unpublished report. IMEDEA UIB-CSIC. Mallorca, Spain, pp. 25-32.

Knudsen, M. D. 1987. Recovery of endangered and threatened plants in California: The federal role. In Elias, T. (Ed.), Conservation and management of rare and endangered plants. California Native Plant Society, Sacramento, California, USA, pp. 461-469.

Koltunow, A.M., Grossniklaus, U. 2003. Apomixis: a developmental perspective. Annual Review of Plant Biology 54, 547-574.

Kondrashov, A.S. 1993. Classification of hypothesis on the advantage of amphimixis. Journal of Heredity 84 (5), 372-387.

Laguna, E., Deltoro, V.I., Perez-Botella, J., Perez-Rovira, P., Serra, L., Olivares, A., Fabregat, C. 2004. The role of small reserves in plant conservation in a region of high diversity in eastern Spain. Biological Conservation 119 (3), 421-426.

Lesica, P., Allendorf, F.W. 1992. Are small populations of plants worth preserving? Conservation Biology 6 (1), 135-139.

Luzuriaga, A. L., Escudero, A., Pérez-Garciá, F. 2006. Environmental maternal effects on seed morphology and germination in Sinapis arvensis (Cruciferae). Weed research 46 (2), 163-174.

Martínez-Duro, E., Ferrandis, P., Herranz, J.M., Copete, M.A. 2010. Do seed harvesting ants threaten the viability of a critically endangered non-myrmecochorous perennial plant population? A complex interaction. Population Ecology 52 (3), 397-405.

Maynard Smith J. 1978. The Evolution of Sex. Cambridge University Press, Cambridge. UK.

Medail, F., Quezel, P., 1997. Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin. Annals of the Missouri Botanical Garden 84 (1), 112-127.

Michaels, H.J., Bazzaz, F.A. 1986. Resource allocation and demography of sexual and apomictic Antennaria parlinii. Ecology 67, 27–36.

Navascués, M., Stoeckel. S., Mariette. S. 2010. Genetic diversity and fitness in small populations of partially asexual, self-incompatible plants. Heredity 104 (5), 482-492.

Paolini, R., Principi, M., Froud-Williams, R.J., Del Plugia, S., Biancardi, E. 1999. Competition between sugarbeet and Sinapis arvensis and Chenopodium album, as affected by timing of nitrogen fertilization. Weed Research 39, 425–440.

Pavlik, B.M., Nickrent, D.L., Howald, A.M. 1993. The recovery of an endangered plant. I. Creating a new population of Amsinckia grandiflora. Conservation Biology 7 (3), 510-526.

Primack, R., Drayton, B. 1997. The experimental ecology of reintroduction. Plant Talk October 25–28.

R Development Core Team. 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. [Available from http://www.R-project.org].

Retana, J., Pico, F.X., Rodrigo, A. 2004. Dual role of harvesting ants as seed predators and dispersers of a non-myrmechorous Mediterranean perennial herb. Oikos 105 (2), 377-385.

Roach, D.A., Wulff, R. D. 1987. Maternal effects in plants. Annual Review of Ecology and Systematics 18, 209-235.

Rosselló, J.A. i Sáez, L. 2004. Limonium barceloi Gil i Llorens, in: Bañares, A., Blanca, G., Güelmes, J., Moreno, J. C., Ortiz, S. (Eds.), Atlas y Libro Rojo de la Flora Vascular Amenazada de España. Tragsa-Ministerio de Medio Ambiente. Spain, pp. 340-341.

Rosselló, J. A. 2008. Relacions taxonòmiques i evolutives entre diverses espècies de saladines endèmiques de Balears. Jardí Botànic, Universitat de Valencia, Spain.

Sáez, L., Rosselló, J.A. 2001. Llibre Vermell de la Flora Vascular de les Illes Balears. Documents Tècnics de Conservació II (9). Conselleria de Medi Ambient. Govern de les Illes Balears, Spain.

Sammut, P. 2008. Three Coleophoridae species new to the lepidopterofauna of the Maltese Islands and one new to the fauna of Europe (Lepidoptera: Coleophoridae). SHILAP Revta. lepid. 36 (141), 5-7.

Schemske, D.W., Husband, B.C., Ruckelshaus, M.H., Goodwillie, C., Parker, I., Bishop, J.G. 1994. Evaluating approaches to the conservation of rare and endangered plants. Ecology 75, 584–606.

Simberloff, D. 1988. The contribution of population and community biology to conservation science. Annual Review of Ecology and Systematics 19, 473-511.

Stanton, M.L. 1984. Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 65, 1105–1112.

Tucker, M., Araujo, A., Paech, N., Hecht, V., Schmidt, E., Rossell, J., de Vries, S., Koltunow, A. 2003. Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. The Plant Cell 15, 1524–1537.

Vander Wall, S.B., Kuhn, K.M., Beck, M.J. 2005. Seed removal, seed predation, and secondary dispersal. Ecology 86, 801–806.

Van Dijk, P.J. 2007. Potential and realized costs of sex in dandelions, Taraxacum officinale s.l., in: Hörandl, E., Grossniklaus, U., Van Dijk, P.J., Sharbel, T. (Eds.), Apomixis: evolution, mechanisms and perspectives. Gantner, Ruggell, Liechtenstein, Germany, pp. 215–233.

Vicens, M., Bibiloni, G., 2007. Pla de recuperació de Limonium barceloi Gil & Llorens. Conselleria de Medi Ambient. Govern de les Illes Balears. Spain.

Voigt, M.L., Melzer, M., Rutten, T., Mitchell-Olds, T., Sharbel, T.F. 2007. Gametogenesis in the apomictic Boechera holboellii complex: the male perspective, in: Hörandl, E., Grossniklaus, U., Van Dijk, P.J., Sharbel, T. (Eds.), Apomixis: evolution, mechanisms and perspectives. Gantner, Ruggell, Liechtenstein, Germany, pp 235–258.

White, J.P., Robertson, I.C. 2009. Intense seed predation by harvester ants on a rare mustard. Ecoscience 16 (4), 508-513.

Whitten, A. J. 1990. Recovery: a proposed programme for Britain's protected species. CSD Report No. 1089. Nature Conservancy Council, Peterborough, UK.

Whitton, J., Sears, C.J., Baack, E.J., Otto, S.P. 2008. The dynamic nature of apomixis in the angiosperms. International Journal of Plant Sciences 169 (1), 169-182.

Table 1.

Floral visitors to Limonium barceloi and visitation rates 2009-2010.

Fig. 1

Fig. 2