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Analysis of climate changes, habitat fragmentation and germination behavior in Muscari gussonei, Petagnaea gussonei and Poterium spinosum, three Mediterranean plants of conservation interest


Abstract

Knowing the optimum germination temperatures of endangered plants, as well as the magnitude of climate changes (e.g., rising temperatures) across the spatial range of these species, is essential to assess the level of threat for such species and, consequently, to implement tailored and enduring conservation programs. These analyses should be also integrated by the study of land-cover changes, which can act as an indicator of landscape fragmentation and, therefore, as a proxy of gene flow across metapopulations of species of conservation interest. This study, in particular, investigated both the germination behavior of Muscari gussonei, Petagnaea gussonei and Poterium spinosum, and the trends of climate and land-cover changes occurred in the distributional areas of these species. M. gussonei and P. gussonei are two endangered and narrowly distributed endemic plants from Sicily (Italy), whereas P. spinosum is another biogeographically important species with a highly scattered range across south-eastern Sicily. All the studied plants showed the same narrow germination optimum of 10–15 °C, but different final germination percentage (FGP): 82–98% in M. gussonei, 10–38% in P. gussonei, 5–61% in fruits and 21–68% in seeds of P. spinosum. These optimum germination temperatures are low and limited and, therefore, make the three species much more vulnerable to ever-rising temperatures, which specifically increased by up to 2 °C in the period 1931–2020. Similarly, across the species ranges during 2000–2018, the analysis of CORINE Land Cover classes showed highly fragmented landscapes, where forest and seminatural areas (class 3) declined, and agricultural areas (class 2) increased. The ongoing climate changes will make the suitable germination temperatures harder to be reached by plants with low and narrow germination optimum, such as M. gussonei, P. gussonei and P. spinosum, whose survival is further threatened by a complex fragmented territory with declining natural areas.

Data availability

The data that support the findings of this study are not openly available due to reasons of sensitivity and are available from the corresponding author upon reasonable request. Data are located in controlled access data storage at the Department of Biological, Geological and Environmental Sciences (Catania University, Italy).

References

  1. Greuter, W. Botanical diversity, endemism, rarity and extinction in the Mediterranean area: an analysis based on the published volumes of Med-checklist. Botanika Chronika 10, 63–79 (1991).

    Google Scholar 

  2. Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).

    Google Scholar 

  3. Cuttelod, A., García, N., Abdul Malak, D., Temple, H., Katariya, V. The Mediterranean: a biodiversity hotspot under threat. In The 2008 Review of The IUCN Red List of Threatened Species. (eds. Vié, J.-C., Hilton-Taylor, C., Stuart, S.N.) (IUCN, Gland, Switzerland, 2008).

  4. Fenu, G. et al. Active management actions for the conservation of the endangered mediterranean island flora: the CARE-MEDIFLORA project. Plant Sociol. 54, 101–110 (2017).

    Google Scholar 

  5. Fenu, G. et al. A Common approach to the conservation of threatened Island vascular plants: first results in the Mediterranean basin. Diversity 12(4), 157 (2020).

    Google Scholar 

  6. Médail, F. The specific vulnerability of plant biodiversity and vegetation on Mediterranean islands in the face of global change. Reg. Environ. Chang. 17(2017), 1775–1790 (2017).

    Google Scholar 

  7. Médail, F. Plant biogeography and vegetation patterns of the Mediterranean islands. Bot. Rev. 88, 63–129 (2022).

    Google Scholar 

  8. Blondel, J., Aronson, J., Bodiou, J.-Y. & Boeuf, G. In The Mediterranean Region: Biological Diversity through Time and Space 2nd edn. (Oxford University Press, 2010).

    Google Scholar 

  9. Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W. & Courchamp, F. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15(4), 365–377 (2012).

    Google Scholar 

  10. Ceballos, G. et al. Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).

    Google Scholar 

  11. AllEnvi. The Mediterranean Region under Climate Change (IRD Editions, 2016).

    Google Scholar 

  12. Segan, D. B., Murray, K. A. & Watson, J. E. M. A global assessment of current and future biodiversity vulnerability to habitat loss–climate change interactions. Glob. Ecol. Conserv. 5, 12–21 (2016).

    Google Scholar 

  13. Feeley, K. J., Bravo-Avila, C., Fadrique, B., Perez, T. M. & Zuleta, D. Climate-driven changes in the composition of New World plant communities. Nat. Clim. Chang. 10, 965–970 (2020).

    Google Scholar 

  14. Santiago-Ramos, J. & Feria-Toribio, J. M. Assessing the effectiveness of protected areas against habitat fragmentation and loss: a long-term multi-scalar analysis in a Mediterranean region. J. Nat. Conserv. 64, 126072 (2021).

    Google Scholar 

  15. Ranal, M. A. & Santana, D. G. How and why to measure the germination process?. Braz. J. Bot. 29, 1–11 (2006).

    Google Scholar 

  16. Bonanno, G. & Veneziano, V. Rise, fall and hope for the Sicilian endemic plant Muscari gussonei: a story of survival in the face of narrow germination optimum, climate changes, desertification and habitat fragmentation. Sci. Total Environ. 912(C), 169208 (2024).

    Google Scholar 

  17. Bonanno, G. & Veneziano, V. Seed dormancy, climate changes, desertification and soil use transformation threaten the Mediterranean endemic monospecific plant Petagnaea gussonei. Sci. Rep. 14, 8235 (2024).

    Google Scholar 

  18. Bonanno, G. & Veneziano, V. Intrapopulation germinability may help the Mediterranean plant species Poterium spinosum L. to cope with climate changes and landscape fragmentation. Sci. Rep. 14, 22235 (2024).

    Google Scholar 

  19. Gargano, D., Fenu, G., Medagli, P., Sciandrello, S. & Bernardo, L. The status of Sarcopoterium spinosum (Rosaceae) at the western periphery of its range: ecological constraints lead to conservation concerns. Israel J. Plant Sci. 55, 1–13 (2007).

    Google Scholar 

  20. De Castro, O. et al. Old sleeping sicilian beauty: seed germination in the palaeoendemic Petagnaea gussonei (Spreng.) Rauschert (Saniculoideae, Apiaceae). Plant. Biol. 17, 1095–1098 (2015).

    Google Scholar 

  21. Salmeri, C. & Trubia, M. Seed germination reports for coastal sand dune species from Sicily. Flora Mediterr. 29, 277–287 (2019).

    Google Scholar 

  22. Gianguzzi, L., La Mantia, A. & Lo Presti, R. M. Distribuzione, ecologia e status conservativo delle stazioni di Petagnaea gussonei (Sprengel) Rauschert (Apiaceae) nell’area dei Monti Nebrodi (Sicilia nord-orientale). Nat. Sicil. 28(1), 265–326 (2004).

    Google Scholar 

  23. Rossi, G. et al. Is legal protection sufficient to ensure plant conservation? the Italian red list of policy species as a case study. Oryx 50(3), 431–436 (2016).

    Google Scholar 

  24. Top 50 Mediterranean Island Plants https://top50.iucn-mpsg.org/species/38 (2017).

  25. Habitats Directive, Council Directive 92/43/EEC on the Conservation of natural habitats and of wild fauna and flora. https://ec.europa.eu/environment/nature/legislation/habitatsdirective/index_en.htm (1992).

  26. Evenari, M. et al. (eds) Ecosystems of the world: Hot deserts and arid shrublands (Elsevier Science Publishers, 1986).

    Google Scholar 

  27. Garbari, F. & Di Martino, A. Leopoldia gussonei Parl. (Liliaceae), specie endemica siciliana. Webbia 27, 89–297 (1972).

    Google Scholar 

  28. Brullo, S. & Marcenò, C. Vulpio-Leopoldietum gussonei ass. nov. dell’Alkanneto-Malcolmion nella Sicilia meridionale. Not. Fitosoc. 8, 75–85 (1974).

    Google Scholar 

  29. Sicilian Regional Government. Meteorological records. https://www.regione.sicilia.it/istituzioni/regione/strutture-regionali/presidenza-regione/autorita-bacino-distretto-idrografico-sicilia/annali-idrologici (2022).

  30. APG. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot. J. Linnean Soc. 161, 105–121 (2009).

    Google Scholar 

  31. WCSP, World checklist of selected plant families. facilitated by the royal botanic gardens, kew. Published on the Internet: http://wcsp.science.kew.org (2021).

  32. Orsenigo, S. et al. Red listing plants under full national responsibility: extinction risks and threats in the vascular flora endemic to Italy. Biol. Conserv. 224, 213–222 (2018).

    Google Scholar 

  33. Wolff, H. Umbelleferae–Saniculoideae, In Wilhelm Engelmann (Ed. Engler, A.), Das Pflanzenreich IV, 228 (Hf. 61). pp 1–305 [Petagnaea in pp. 23, 273–274] (Leipzig, Germany, 1913).

  34. Calviño, C. I. & Downie, S. R. Circumscription and phylogeny of apiaceae subfamily saniculoideae based on chloroplast DNA sequences. Mol. Phylogenet. Evol. 44, 175–191 (2007).

    Google Scholar 

  35. Calviño, C. I., Martínez, S. G. & Downie, S. R. Morphology and biogeography of apiaceae subfamily Saniculoideae as inferred by phylogentic analysis of molecular data. Am. J. Bot. 95(2), 196–214 (2008).

    Google Scholar 

  36. Kadereit, J. W., Repplinger, M., Schmalz, N., Uhink, C. H. & Wörz, A. The phylogeny and biogeography of apiaceae subf. saniculoideae tribe saniculeae: from south to north and south again. Taxon 57, 365–382 (2008).

    Google Scholar 

  37. De Castro, O., Cennamo, P. & De Luca, P. Analysis of the genus Petagnaea Caruel (Apiaceae), using new molecular and literature data. Plant Syst. Evolut. 278(3), 239–249 (2009).

    Google Scholar 

  38. Gianguzzi, L. Petagnaea gussonei (Sprengel) Rauschert. schede per una Lista Rossa della Flora vascolare e crittogamica Italiana. Inf. Botanico Italiano 43(2), 412–416 (2011).

    Google Scholar 

  39. Pignatti, S. Flora d’Italia (Edagricole, 1982).

    Google Scholar 

  40. SINANET, CORINE Land Cover. https://groupware.sinanet.isprambiente.it/uso-copertura-e-consumo-di-suolo/library/copertura-del-suolo/corine-land-cover (2018).

  41. Bacchetta, G., Fenu, G., Mattana, E., Piotto, B., Virevaire, M. Manuale per la raccolta, studio, conservazione e gestione ex situ del germoplasma. Manuali e Linee Guida APAT 37/2006, APAT, Roma (2006).

  42. Bacchetta, G., Fenu, G., Mattana, E., Piotto B. Procedure per il campionamento in situ e la conservazione ex situ del germoplasma. Manuali e linee guida ISPRA, 118/2014.(2014).

  43. ENSCONET Germination Recommendations. Updated (2009).

  44. ISTA. International rules for seed testing 2017 (The International Seed Testing Association (ISTA), 2017).

    Google Scholar 

  45. Scott, S., Jones, R. & Williams, W. Review of data analysis methods for seed germination. Crop Sci. 24, 1192–1199 (1984).

    Google Scholar 

  46. Orchard, T. Estimating the parameters of plant seedling emergence. Seed Sci. Technol. 5, 61–69 (1977).

    Google Scholar 

  47. Al-Mudaris, M. A. Notes on various parameters recording the speed of seed germination. J. Agric. Trop. Subtrop. 99, 147–154 (1998).

    Google Scholar 

  48. Coolbear, P., Francis, A. & Grieson, D. The effect of low temperature pre-sowing treatment on the germination performance and membrane integrity of artificially aged tomato seeds. J. Exp. Bot. 35(160), 1609–1617 (1984).

    Google Scholar 

  49. Jones, K. & Sanders, D. The influence of soaking pepper seed in water or potassium salt solutions on germination at three temperatures. J. Seed Technol. 11, 97–102 (1987).

    Google Scholar 

  50. Lionello, P., Giorgi, F., Rohling, E. & Seager, R. Medi terranean climate: past, present and future (chapter 3). In Oceanography of the Mediterranean Sea (eds Schroeder, K. & Chiggiato, J.) 41–91 (Elsevier, 2022).

    Google Scholar 

  51. Baskin, C. C. & Baskin, J. M. Seeds: Ecology, biogeography, and evolution of dormancy and germination 2nd edn. (Academic Press, 2014).

    Google Scholar 

  52. Thanos, C. A., Georghiou, K., Dimitra, J. D. & Marangaki, C. J. Photoinhibition of seed germination in Mediterranean maritime plants. Ann. Bot. 68, 469–475 (1991).

    Google Scholar 

  53. Thanos, C. A., Kadis, C. C. & Skarou, F. Ecophysiology of germination in the aromatic plants thyme, savory and oregano. Seed Sc. Res. 5, 161–170 (1995).

    Google Scholar 

  54. Doussi, M. A. & Thanos, C. A. Ecophysiology of seed germination in Mediterranean geophytes. 1. Muscari Spp. Seed Sci. Res. 12, 193–201 (2002).

    Google Scholar 

  55. Kadis, C. & Georghiou, K. Seed dispersal and germination behavior of three threatened endemic labiates of Cyprus. Plant Species Biol. 25, 77–84 (2010).

    Google Scholar 

  56. Picciau, R., Pritchard, H. W., Mattana, E. & Bacchetta, G. Thermal thresholds for seed germination in Mediterranean species are higher in mountain compared with lowland areas. Seed Sci. Res. 29, 44–54 (2019).

    Google Scholar 

  57. Pearson, R. G. Climate change and the migration capacity of species. Trends Ecol. Evol. 21, 111–113 (2006).

    Google Scholar 

  58. Engler, R. et al. Predicting future distributions of mountain plants under climate change: does dispersal capability matter?. Ecography 32, 34–45 (2009).

    Google Scholar 

  59. Lavergne, S., Thuiller, W., Molina, J. & Debussche, M. Environmental and human factors influencing rare plant local occurrence, extinction and persistence: a 115-year study in the Mediterranean region. J. Biogeogr. 32, 799–811 (2005).

    Google Scholar 

  60. Isik, K. Rare and endemic species: why are they prone to extinction?. Turk. J. Bot. 35, 411–417 (2011).

    Google Scholar 

  61. Fernández-Mazueco, M., Jiménez-Mejías, P., Rotllan-Puig, X. & Vargas, P. Narrow endemics to Mediterranean islands: Moderate genetic diversity but narrow climatic niche of the ancient, critically endangered Naufraga (Apiaceae). Persp. Plant Ecol. Evol. Sys. 16, 190–202 (2014).

    Google Scholar 

  62. Thompson, J. D. Plant evolution in the Mediterranean. Insights for conservation 2nd edition. (Oxford University Press, 2020).

    Google Scholar 

  63. Davis, M. B., Shaw, R. G. & Etterson, J. R. Evolutionary responses to changing climate. Ecology 86, 1704–1714 (2005).

    Google Scholar 

  64. Hansen, M. M., Olivieri, I., Waller, D. M., Nielsen, E. E., The GeM Working Group. Monitoring adaptive genetic responses to environmental change. Mol. Ecol. 21(6), 1311–1329 (2012).

    Google Scholar 

  65. Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520(7545), 45–50 (2015).

    Google Scholar 

  66. Williams, D. R. et al. Proactive conservation to prevent habitat losses to agricultural expansion. Nat. Sustain. 4, 314–322 (2021).

    Google Scholar 

  67. Potapov, P. et al. Global maps of cropland extent and change show accelerated cropland expansion in the twenty-first century. Nat. Food 3, 19–28 (2022).

    Google Scholar 

  68. Matesanz, S., Escudero, A. & Valladares, F. Impact of three global change drivers on a Mediterranean shrub. Ecology 90, 2609–2621 (2009).

    Google Scholar 

  69. Modica, G. et al. Implementation of multispecies ecological networks at the regional scale: analysis and multi-temporal assessment. J. Environ. Manage. 289, 112494 (2021).

    Google Scholar 

  70. Sahraoui, Y. et al. Integrating ecological networks modelling in a participatory approach for assessing impacts of planning scenarios on landscape connectivity. Landsc. 209, 104–39 (2021).

    Google Scholar 

  71. Fenu, G. et al. An early evaluation of translocation actions for endangered plant species on Mediterranean islands. Plant Diver. 41, 94–104 (2019).

    Google Scholar 

  72. Bellis, J. et al. Identifying predictors of translocation success in rare plant species. Conserv. Biol. 38(2), e14190 (2024).

    Google Scholar 

  73. D’Agostino, M. et al. Best practices, errors, and perspectives of half a century of plant translocation in Italy. Conserv. Biol. 38, e14233 (2024).

    Google Scholar 

  74. Fenu, G., Cogoni, D. & Bacchetta, G. The role of fencing in the success of threatened plant species translocation. Plant Ecol. 217(2), 207–217 (2016).

    Google Scholar 

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Funding

This study was partially funded by the Italian Ministry of University and Research, National Operation Program (Programma Operativo Nazionale – PON), Research and Innovation, Green Themes, Action IV. 6. Project Title “Conservation of species and habitats of community importance: seed biology, ex situ and in situ conservation” (D.M. 1062, 10/08/2021). The authors are thankful to all the people who gave assistance during field activities and laboratory experiments.

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The authors declare that they contributed equally to each part of the manuscript. G. B.: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Supervision, Validation, Visualization, Writing original draft, Writing review & editing. V. V.: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Supervision, Validation, Visualization, Writing original draft, Writing review & editing.

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Correspondence to
Giuseppe Bonanno.

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All authors have read, understood, and have complied as applicable with the statement on “Ethical responsibilities of Authors”, as found in the Instructions for Authors.

Plant materials statement

The authors of this paper, Giuseppe Bonanno and Vincenzo Veneziano, undertook the formal identification of all the plant material collected in this study. The permission to collect specimens of Muscari gussonei, Petagnaea gussonei and Poterium spinosum was granted by the Regional Government of Sicily. Plant collection and use were in accordance with the relevant institutional, national and international guidelines and legislation. Specifically, in compliance with the collection permission, all specimens were < 10% of the sampled populations. The authors declare that they complied with the IUCN Policy Statement on Research Involving Species at Risk of Extinction, and the Convention on the Trade in Endangered Species of Wild Fauna and Flora. Voucher specimens were deposited in the public herbarium of the Botanical Garden of Catania University (Italy). Specimens were collected, identified and deposited by the authors of this article.

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Bonanno, G., Veneziano, V. Analysis of climate changes, habitat fragmentation and germination behavior in Muscari gussonei, Petagnaea gussonei and Poterium spinosum, three Mediterranean plants of conservation interest.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-46658-9

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  • DOI: https://doi.org/10.1038/s41598-026-46658-9

Keywords

  • Mediterranean endemic plants
  • Global warming
  • CORINE land cover
  • Germination performance

  • In situ and ex situ conservation
  • Sicily


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