Plant species richness hotspots and related drivers across spatial scales in small Mediterranean islands

Riccardo Testolin1,2,3(), Fabio Attorre4, Vanessa Bruzzaniti1,2,3, Riccardo Guarino5, Borja Jiménez-Alfaro6, Michele Lussu1,2,3, Stefano Martellos2,7, Michele Di Musciano1,8, Salvatore Pasta9, Francesco Maria Sabatini1,10, Francesco Santi1, Piero Zannini1,2,3, Alessandro Chiarucci1

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Journal of Systematics and Evolution ›› 2024, Vol. 62 ›› Issue (2) : 242-256. DOI: 10.1111/jse.13034
Research Article

Plant species richness hotspots and related drivers across spatial scales in small Mediterranean islands

  • Riccardo Testolin1,2,3(), Fabio Attorre4, Vanessa Bruzzaniti1,2,3, Riccardo Guarino5, Borja Jiménez-Alfaro6, Michele Lussu1,2,3, Stefano Martellos2,7, Michele Di Musciano1,8, Salvatore Pasta9, Francesco Maria Sabatini1,10, Francesco Santi1, Piero Zannini1,2,3, Alessandro Chiarucci1
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Abstract

Small islands represent a common feature in the Mediterranean and host a significant fraction of its biodiversity. However, the distribution of plant species richness across spatial scales—from local communities (alpha) to whole islands (gamma)—is largely unknown, and so is the influence of environmental, geographical, and topographical factors. By building upon classic biogeographic theory, we used the species–area relationship and about 4500 vegetation plots in 54 Central Mediterranean small islands to identify hotspots of plant species richness and the underlying spatial determinants across scales. To do so, we fitted and averaged eight species–area models on gamma and alpha richness against island area and plot size, respectively. Based on positive deviations from the fitted curves, we identified 12 islands as cross-scale hotspots. These islands encompassed around 70% of species and habitat richness, as well as almost 50% of the rarest species in the data set, while occupying less than 40% of the total island surface. By fitting generalized linear mixed models, we found that gamma richness was mainly explained by island area and was weakly related to mean annual temperature (positively) and annual precipitation (negatively). As for alpha richness, after accounting for the idiosyncratic effect of habitats and islands, plot size and gamma richness remained the only significant predictors, showing a positive relationship. This work contributes to the understanding of the patterns and drivers of plant diversity in Central Mediterranean small islands and outlines a useful methodology for the prioritization of conservation efforts.

Keywords

biodiversity hotspots / conservation biogeography / species–area relationship / vascular plants / vegetation plots

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Riccardo Testolin, Fabio Attorre, Vanessa Bruzzaniti, Riccardo Guarino, Borja Jiménez-Alfaro, Michele Lussu, Stefano Martellos, Michele Di Musciano, Salvatore Pasta, Francesco Maria Sabatini, Francesco Santi, Piero Zannini, Alessandro Chiarucci. Plant species richness hotspots and related drivers across spatial scales in small Mediterranean islands. Journal of Systematics and Evolution, 2024, 62(2): 242‒256 https://doi.org/10.1111/jse.13034

References

1 N Alessi, V Bruzzaniti, F Buldrini, E Centomo, M Cervellini, M Enea, S Landi, C Lelli, I Montanari, J Nascimbene, G Pezzi, G Virzí, P Zannini, A Chiarucci. 2022. AMS-VegBank: A new database of vegetation plots for the Italian territory. Vegetation Classification and Survey 3: 177–185.
2 C Barboutis, E Navarrete, G Karris, S Xirouchakis, T Fransson, A Bounas. 2022. Arriving depleted after crossing of the Mediterranean: Obligatory stopover patterns underline the importance of Mediterranean islands for migrating birds. Animal Migration 9: 27–36.
3 K Bartoń. 2022. MuMIn: Multi-Model Inference. R package version 1.46.0.
4 D Bates, M Mächler, BM Bolker, SC Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.
5 PAV Borges, P Cardoso, R Gabriel, C Ah-Peng, BC Emerson. 2016. Challenges, advances and perspectives in island biogeography. Frontiers of Biogeography 8(2): e29136.
6 H Bruelheide, B Jiménez-Alfaro, U Jandt, FM Sabatini. 2020. Deriving site-specific species pools from large databases. Ecography 43: 1215–1228.
7 H Bruelheide, L Tichý, M Chytrý, F Jansen. 2021. Implementing the formal language of the vegetation classification expert systems (ESy) in the statistical computing environment R. Applied Vegetation Science 24: 1–7.
8 S Brullo. 1985. Sur la syntaxonomie des pelouses thérophytiques des territoires steppiques de l′Europe sud-occidentale. Documents Phytosociologiques 9: 1–17.
9 EM Cañadas, G Fenu, J Peñas, J Lorite, E Mattana, G Bacchetta. 2014. Hotspots within hotspots: Endemic plant richness, environmental drivers, and implications for conservation. Biological Conservation 170: 282–291.
10 A Carta, L Forbicioni, G Frangini, B Pierini, L Peruzzi. 2018. An updated inventory of the vascular flora of Elba island (Tuscan Archipelago, Italy). Italian Botanist 6: 1–22.
11 A Chao. 1987. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43: 783–791.
12 A Chao, NJ Gotelli, TC Hsieh, EL Sander, KH Ma, RK Colwell, AM Ellison. 2014. Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45–67.
13 A Chiarucci, F Buldrini, M Cervellini, R Guarino, M Caccianiga, B Foggi, D Viciani, L Lazzaro, L Casella, P Angelini, BEL Cerabolini, S Pasta, M Enea, P Zannini. 2021. Habitat type and island identity as drivers of community assembly in an archipelago. Journal of Vegetation Science 32: jvs.12953.
14 A Chiarucci, S Fattorini, B Foggi, S Landi, L Lazzaro, J Podani, D Simberloff. 2017. Plant recording across two centuries reveals dramatic changes in species diversity of a Mediterranean archipelago. Scientific Reports 7: 5415.
15 A Chiarucci, R Guarino, S Pasta, A La Rosa, P Lo Cascio, F Médail, D Pavon, JM Fernández-Palacios, P Zannini. 2021. Species–area relationship and small-island effect of vascular plant diversity in a young volcanic archipelago. Journal of Biogeography 48: 2919–2931.
16 M Chytrý, L Tichý, SM Hennekens, I Knollová, JAM Janssen, JS Rodwell, T Peterka, C Marcenò, F Landucci, J Danihelka, M Hájek, J Dengler, P Novák, D Zukal, B Jiménez-Alfaro, L Mucina, S Abdulhak, S Aćić, E Agrillo, F Attorre, E Bergmeier, I Biurrun, S Boch, J Bölöni, G Bonari, T Braslavskaya, H Bruelheide, JA Campos, A Čarni, L Casella, M Ćuk, R Ćušterevska, E De Bie, P Delbosc, O Demina, Y Didukh, D Dziuba Dítě, J Ewald, RG Gavilán, J-C Gégout, GP Giusso del Galdo, V Golub, N Goncharova, F Goral, U Graf, A Indreica, M Isermann, U Jandt, F Jansen, J Jansen, A Jašková, M Jiroušek, Z Kącki, V Kalníková, A Kavgacı, L Khanina, AY Korolyuk, M Kozhevnikova, A Kuzemko, F Küzmič, OL Kuznetsov, M Laiviņš, I Lavrinenko, O Lavrinenko, M Lebedeva, Z Lososová, T Lysenko, L Maciejewski, C Mardari, A Marinšek, MG Napreenko, V Onyshchenko, A Pérez-Haase, R Pielech, V Prokhorov, V Rašomavičius, MP Rodríguez Rojo, S Rūsiņa, J Schrautzer, J Šibík, U Šilc, Ž Škvorc, VA Smagin, Z Stančić, A Stanisci, E Tikhonova, T Tonteri, D Uogintas, M Valachovič, K Vassilev, D Vynokurov, D Willner, S Yamalov, D Evans, M Palitzsch Lund, R Spyropoulou, E Tryfon, JHJ Schaminée. 2020. EUNIS Habitat Classification: Expert system, characteristic species combinations and distribution maps of European habitats. Applied Vegetation Science 23: 648–675.
17 RM Cowling, PW Rundel, BB Lamont, MK Arroyo, M Arianoutsou. 1996. Plant diversity in Mediterranean-climate regions. Trends in Ecology and Evolution 11: 362–366.
18 M de Cáceres, X Font, F Oliva. 2010. The management of vegetation classifications with fuzzy clustering. Journal of Vegetation Science 21: 1138–1151.
19 A Deidun. 2010. Challenges to the conservation of biodiversity on small islands: The case of the Maltese Islands. International Journal of Arts and Sciences 3: 175–187.
20 V Devictor, D Mouillot, C Meynard, F Jiguet, W Thuiller, N Mouquet. 2010. Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: The need for integrative conservation strategies in a changing world. Ecology Letters 13: 1030–1040.
21 M Everton. 2023. rrindex: Calculating the rarity index by species. R package version 0.0.0.9000.
22 TG Farr, PA Rosen, E Caro, R Crippen, R Duren, S Hensley, M Kobrick, M Paller, E Rodriguez, L Roth, D Seal, S Shaffer, J Shimada, J Umland, M Werner, M Oskin, D Burbank, DE Alsdorf. 2007. The shuttle radar topography mission. Reviews of Geophysics 45: 1–33.
23 S Fattorini. 2006. Detecting biodiversity hotspots by species-area relationships: A case study of Mediterranean beetles. Conservation Biology 20: 1169–1180.
24 S Fattorini. 2021. The identification of biodiversity hotspots using the species–area relationship. In: Matthews TJ, Triantis KA, Whittaker RJ eds. The species-area relationship: Theory and application. Cambridge: Cambridge University Press. 321–344
25 HS Fischer. 2015. On the combination of species cover values from different vegetation layers. Applied Vegetation Science 18: 169–170.
26 G Galasso, F Conti, L Peruzzi, NMG Ardenghi, E Banfi, L Celesti-Grapow, A Albano, A Alessandrini, G Bacchetta, S Ballelli, M Bandini Mazzanti, G Barberis, L Bernardo, C Blasi, D Bouvet, M Bovio, L Cecchi, E Del Guacchio, G Domina, S Fascetti, L Gallo, L Gubellini, A Guiggi, D Iamonico, M Iberite, P Jiménez-Mejías, E Lattanzi, D Marchetti, E Martinetto, RR Masin, P Medagli, NG Passalacqua, S Peccenini, R Pennesi, B Pierini, L Podda, L Poldini, F Prosser, FM Raimondo, F Roma-Marzio, L Rosati, A Santangelo, A Scoppola, S Scortegagna, A Selvaggi, F Selvi, A Soldano, A Stinca, RP Wagensommer, T Wilhalm, F Bartolucci. 2018. An updated checklist of the vascular flora alien to Italy. Plant Biosystems 152: 556–592.
27 NJ Gotelli, RK Colwell. 2011. Estimating species richness. In: Magurran AE, McGill BJ eds. Biological diversity: Frontiers in measurement and assessment. Oxford: Oxford University Press. 39–54.
28 W Greuter. 1995. Origin and peculiarities of Mediterranean island floras. Ecologia Mediterranea 21: 1–10.
29 R Guarino, M Guccione, F Gillet. 2022. Plant communities, synusiae and the arithmetic of a sustainable classification. Vegetation Classification and Survey 3: 7–13.
30 R Guarino, W Willner, S Pignatti, F Attorre, JJ Loidi. 2018. Spatio-temporal variations in the application of the Braun-Blanquet approach in Europe. Phytocoenologia 48: 239–250.
31 F Guilhaumon, A Basset, E Barbone, D Mouillot. 2012. Species-area relationships as a tool for the conservation of benthic invertebrates in Italian coastal lagoons. Estuarine, Coastal and Shelf Science 114: 50–58.
32 F Guilhaumon, O Gimenez, KJ Gaston, D Mouillot. 2008. Taxonomic and regional uncertainty in species-area relationships and the identification of richness hotspots. Proceedings of the National Academy of Sciences of the United States of America 105: 15458–15463.
33 XA Harrison. 2014. Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2: e616.
34 F Hartig. 2022. DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.5.
35 R Hofrichter. 2001. Das Mittelmeer: Fauna, Flora, Ökologie. Heidelberg: Spektrum Akademischer Verlag.
36 TC Hsieh, KH Ma, A Chao. 2020. iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.20.
37 B Jiménez-Alfaro, S Abdulhak, F Attorre, A Bergamini, ML Carranza, A Chiarucci, R Ćušterevska, S Dullinger, RG Gavilán, G Giusso del Galdo, N Kuzmanović, P Laiolo, J Loidi, GP Malanson, C Marcenó, Đ Milanović, ER Pansing, JV Roces-Díaz, E Ruprecht, Ruprecht, J Šibik, A Stanisci, R Testolin, J-P Theurillat, K Vassilev, W Willner, M Winkler. 2021. Post-glacial determinants of regional species pools in alpine grasslands. Global Ecology and Biogeography 30: 101–1115.
38 P Kareiva, M Marvier. 2003. Conserving biodiversity coldspots: Recent calls to direct conservation funding to the world′s biodiversity hotspots may be bad investment advice. American Scientist 91: 344–351.
39 DN Karger, O Conrad, J Böhner, T Kawohl, H Kreft, RW Soria-Auza, NE Zimmermann, HP Linder, M Kessler. 2017. Climatologies at high resolution for the earth′s land surface areas. Scientific Data 4: 170122.
40 DN Karger, O Conrad, J Böhner, T Kawohl, H Kreft, RW Soria-Auza, NE Zimmermann, HP Linder, M Kessler. 2021. Climatologies at high resolution for the earth′s land surface areas. EnviDat [online]. Available from [accessed 4 April 2023].
41 K Kougioumoutzis, A Tiniakou. 2015. Ecological factors driving plant species diversity in the South Aegean Volcanic Arc and other central Aegean islands. Plant Ecology and Diversity 8: 173–186.
42 H Kreft, W Jetz, J Mutke, G Kier, W Barthlott. 2008. Global diversity of island floras from a macroecological perspective. Ecology Letters 11: 116–127.
43 AS Kukkala, A Moilanen. 2013. Core concepts of spatial prioritisation in systematic conservation planning. Biological Reviews 88: 443–464.
44 WT Langford, A Gordon, L Bastin, SA Bekessy, MD White, G Newell. 2011. Raising the bar for systematic conservation planning. Trends in Ecology & Evolution 26: 634–640.
45 MV Lomolino. 2000a. A call for a new paradigm of island biogeography. Global Ecology & Biogeography 9: 1–6.
46 MV Lomolino. 2000b. Ecology′s most general, yet protean pattern: The species-area relationship. Journal of Biogeography 27: 17–26.
47 RH MacArthur, EO Wilson. 1967. The theory of island biogeography. Princeton: Princeton University Press.
48 EA Maciel. 2021. An index for assessing the rare species of a community. Ecological Indicators 124: 107424.
49 B Maitner, B Boyle. 2022. TNRS: Taxonomic Name Resolution Service. R package version 0.3.0.
50 CR Margules, RL Pressey. 2000. Systematic conservation planning. Nature 405: 243–253.
51 TJ Matthews, KA Triantis, RJ Whittaker, F Guilhaumon. 2019. sars: An R package for fitting, evaluating and comparing species–area relationship models. Ecography 42: 1446–1455.
52 F Mazel, F Guilhaumon, N Mouquet, V Devictor, D Gravel, J Renaud, MV Cianciaruso, R Loyola, JAF Diniz-Filho, D Mouillot, W Thuiller. 2014. Multifaceted diversity-area relationships reveal global hotspots of mammalian species, trait and lineage diversity. Global Ecology and Biogeography 23: 836–847.
53 P Mazzola, A Geraci, FM Raimondo. 2001. Endemismo e biodiversità floristica nelle isole circumsiciliane. Biogeographia—The Journal of Integrative Biogeography 22: 1–19.
54 F Médail. 2017. The specific vulnerability of plant biodiversity and vegetation on Mediterranean islands in the face of global change. Regional Environmental Change 17: 1775–1790.
55 F Médail. 2022. Plant biogeography and vegetation patterns of the Mediterranean islands. Botanical Review 88: 63–129.
56 F Médail, P Quézel. 1997. Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin. Annals of the Missouri Botanical Garden 84: 112–127.
57 F Médail, P Quézel. 1999. Biodiversity hotspots in the Mediterranean basin: Setting global conservation priorities. Conservation Biology 13: 1510–1513.
58 R Mittermeier, GP Robles, M Hoffmann, J Pilgrim, T Brooks, C Mittermeier, J Lamoreux, G daFonseca. 2004. Hotspots revisited: Earth's biologically richest and most endangered ecoregions. Mexico City: CEMEX.
59 LW Morrison. 2011. Why do some small islands lack vegetation? Evidence from long-term introduction experiments. Ecography 34: 384–391.
60 D Moss. 2008. EUNIS habitat classification–A guide for users [online]. Available from [accessed 13 August 2023].
61 N Myers, RA Mittermeier, CG Mittermeier, GAB Da Fonseca, J Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858.
62 NASA & JPL. 2013. NASA shuttle radar topography mission global 1 arc second number [SRTMGL1N_003]. NASA EOSDIS Land Processes DAAC [online]. Available from [accessed 2 February 2023].
63 AKJ Niskanen, RK Heikkinen, H Väre, M Luoto. 2017. Drivers of high-latitude plant diversity hotspots and their congruence. Biological Conservation 212: 288–299.
64 CDL Orme, RG Davies, M Burgess, F Eigenbrod, N Pickup, VA Olson, AJ Webster, TS Ding, PC Rasmussen, RS Ridgely, AJ Stattersfield, PM Bennett, TM Blackburn, KJ Gaston, IPF Owens. 2005. Global hotspots of species richness are not congruent with endemism or threat. Nature 436: 1016–1019.
65 EV Perrino, V Tomaselli, R Costa, P Pavone. 2013. Conservation status of habitats (Directive 92/43 EEC) of coastal and low hill belts in a Mediterranean biodiversity hot spot (Gargano—Italy). Plant Biosystems 147: 1006–1028.
66 S Petit, A Abreu, P Emmanouilidou, K Hogg. 2022. Living islands, for a sustainable Mediterranean biodiversity (re)connecting nature and resilient communities. Gland: IUCN.
67 R Core Team. 2022. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
68 RE Ricklefs. 1987. Community diversity: Relative roles of local and regional processes. Science 235: 167–171.
69 FM Sabatini, B Jiménez-Alfaro, U Jandt, M Chytrý, R Field, M Kessler, J Lenoir, F Schrodt, SK Wiser, MAS Arfin Khan, F Attorre, L Cayuela, M De Sanctis, J Dengler, S Haider, MZ Hatim, A Indreica, F Jansen, A Pauchard, RK Peet, P Petřík, VD Pillar, B Sandel, M Schmidt, Z Tang, P van Bodegom, K Vassilev, C Violle, E Alvarez-Davila, P Davidar, J Dolezal, B Hérault, A Galán-de-Mera, J Jiménez, S Kambach, S Kepfer-Rojas, H Kreft, F Lezama, R Linares-Palomino, A Monteagudo Mendoza, JK N'Dja, OL Phillips, G Rivas-Torres, P Sklenář, K Speziale, BJ Strohbach, R Vásquez Martínez, H-F Wang, K Wesche, H Bruelheide. 2022. Global patterns of vascular plant alpha diversity. Nature Communications 13: 4683.
70 S Sfenthourakis, M Panitsa. 2012. From plots to islands: Species diversity at different scales. Journal of Biogeography 39: 750–759.
71 A Stanisci, S Feola, C Blasi. 2005. Map of vegetation series of Ponza island (central Italy). Lanzaroa 26: 93–113.
72 SA Temple. 1981. Applied island biogeography and the conservation of endangered island birds in the Indian Ocean. Biological Conservation 20: 147–161.
73 R Testolin, F Attorre, P Borchardt, RF Brand, H Bruelheide, M Chytrý, M De Sanctis, J Dolezal, M Finckh, S Haider, A Hemp, U Jandt, M Kessler, AY Korolyuk, J Lenoir, N Makunina, GP Malanson, DB Montesinos-Tubée, J Noroozi, A Nowak, RK Peet, G Peyre, FM Sabatini, J Šibík, P Sklenář, SP Sylvester, K Vassilev, R Virtanen, W Willner, SK Wiser, EG Zibzeev, B Jiménez-Alfaro. 2021. Global patterns and drivers of alpine plant species richness. Global Ecology and Biogeography 30: 1218–1231.
74 KA Triantis, F Guilhaumon, RJ Whittaker. 2012. The island species-area relationship: Biology and statistics. Journal of Biogeography 39: 215–231.
75 A Troia. 2012. Insular endemism in the Mediterranean vascular flora: The case of the Aeolian Islands (Sicily, Italy). Biodiversity Journal 3: 369–374.
76 JA Veech. 2000. Choice of species-area function affects identification of hotspots. Conservation Biology 14: 140–147.
77 J Villarreal-Rosas, LJ Sonter, RK Runting, S López-Cubillos, MC Dade, HP Possingham, JR Rhodes. 2020. Advancing systematic conservation planning for ecosystem services. Trends in Ecology & Evolution 35: 1129–1139.
78 U Werner, J Buszko. 2005. Detecting biodiversity hotspots using species-area and endemics-area relationships: The case of butterflies. Biodiversity and Conservation 14: 1977–1988.
79 RJ Whittaker, MB Araújo, P Jepson, RJ Ladle, JEM Watson, KJ Willis. 2005. Conservation biogeography: Assessment and prospect. Diversity and Distributions 11: 3–23.
80 JB Wilson, RK Peet, J Dengler, M Pärtel. 2012. Plant species richness: The world records. Journal of Vegetation Science 23: 796–802.
81 L Zhao, J Li, H Liu, H Qin. 2016. Distribution, congruence, and hotspots of higher plants in China. Scientific Reports 6: 19080.
82 M Zobel. 2016. The species pool concept as a framework for studying patterns of plant diversity. Journal of Vegetation Science 27: 8–18.
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