We applied a multi-taxa approach integrating the co-occurrence of plants, ground beetles, spiders and springtails with soil parameters (temperatures and chemical characteristics) in order to describe the primary succession along two glacier forelands in the Maritime Alps (Italy), a hotspot of Mediterranean biodiversity. We compared these successions to those from Central Alps: Maritime glacier forelands markedly differ for their higher values of species richness and species turnover. Contrary to our expectation, Maritime glacier forelands follow a ‘replacement change model’, like continental succession of Inner Alps and differently from other peripheral successions. We propose that the temperatures along these Mediterranean glacier forelands are warmer than those along other Alpine glacier forelands, which promote the faster species turnover. Furthermore, we found that early and mid successional stages of the investigated glaciers are richer in cold-adapted and endemic species than the later ones: we confirmed that the ‘replacement change’ model disadvantages pioneer, cold-adapted species. Given the overall correspondence among cold-adapted and endemic species, the most threatened in this climate phase, our results raise new concerns about the extinction risk of these species. We also describe supraglacial habitat of Maritime glaciers demonstrating that supraglacial debris represents an environment decoupled from the regional climate and may have an important role as refugium for coldadapted and hygrophilous plant and animal species, whose survival can be threatened by climate change and by a rapid ecological succession in the adjacent forelands.
Bartolucci F, Peruzzi L, Galasso G, et al. (2018) An updated checklist of the vascular flora native to Italy. Plant Biosyst - Int J Deal Asp Plant Biol 152: 179–303. https://doi.org/10.1080/11263504.2017.1419996
Bell JR, Bohan DA, Shaw EM, et al. (2005) Ballooning dispersal using silk: world fauna, phylogenies, genetics and models. Bull Entomol Res 95: 69–114. https://doi.org/10.1079/BER2004350
Bisio L (2008) Second contribute to the knowledge of Piedmont and Aosta Valley Oreonebria: O. castanea and the species of the group “picea” (Coleoptera Carabidae (Secondo contributo alla conoscenza di Oreonebria del Piemonte e della Valle d’Aosta: Oreonebria castanea e le specie del gruppo “picea” (Coleoptera Carabidae).) Riv Piem Sc Nat 29: 177–209. (in Italian)
Bisio L, Taglianti AV (2021) Carabid beetles from Valle Stura di Demonte (Maritime and Cottian Alps (I Carabidi della Valle Stura di Demonte (Alpi Marittime e Cozie)). Boll Della Soc Entomol Ital 153: 51–86. (in Italian)
Bretfeld G (1999) Symphypleona, Synopses on Palaearctic Collembola. Senckenberg Museum of Natural History Görlitz.
Burga CA (1999) Vegetation development on the glacier foreland Morteratsch (Switzerland). Appl Veg Sci 2: 17–24.
Caccianiga M, Andreis C, Cerabolini B (2001). Vegetation and environmental factors during primary succession on glacier forelands: some outlines from the Italian Alps. Plant Biosyst 135: 295–310. https://doi.org/10.1080/11263500112331350930
Caccianiga M, Andreis C, Diolaiuti G, et al. (2011) Alpine debris-covered glaciers as a habitat for plant life. The Holocene 21: 1011–1020. https://doi.org/10.1177/0959683611400219
Castle SC, Lekberg Y, Affleck D, et al. (2016) Soil abiotic and biotic controls on plant performance during primary succession in a glacial landscape. J Ecol 104: 1555–1565. https://doi.org/10.1111/1365-2745.12615
Cauvy-Fraunié S, Dangles O (2019) A global synthesis of biodiversity responses to glacier retreat. Nat Ecol Evol 3: 1675–1685. https://doi.org/10.1038/s41559-019-1042-8
D’Amico M, Gorra R, Freppaz M 2015. Small-scale variability of soil properties and soil-vegetation relationships in patterned ground on different lithologies (NW Italian Alps). Catena 135: 47–58. https://doi.org/10.1016/j.catena.2015.07.005
Deharveng L, D’Haese CA, Bedos A (2008). Global diversity of springtails (Collembola; Hexapoda) in freshwater. Hydrobiologia 595: 329–338. https://doi.org/10.1007/s10750-007-9116-z
Erschbamer B, Caccianiga M (2016) Glacier Forelands: Lessons of Plant Population and Community Development. Series Progress in Botany 78: 259–284. Springer International Publishing.
Federici PR, Pappalardo M (1995) Recent evolution of the glaciers of the Maritime Alps (L’evoluzione recente dei ghiacciai delle Alpi Marittime.) Geogr Fis Din Quat 18: 257–269. (In Italian)
Federici PR, Pappalardo M (2010) Glacier retreat in the maritime alps area. Geogr. Ann. Ser. Phys. Geogr. 92, 361–373. https://doi.org/10.1111/j.1468-0459.2010.00401.x
Ficetola GF, Marta S, Guerrieri A, et al. (2021) Dynamics of ecological communities following current retreat of glaciers. Ann Rev Ecol Evol Syst 52:405–426. https://doi.org/10.1146/annurev-ecolsys-010521-040017
Gereben-Krenn B-A (1995) Co-occurence and Michrohabitat Distribution of Six Nebria species (Coleoptera: Carabidae) in an Alpine Glacier Retreat Zone in the Alps, Austria. Arct Alp Res 27: 371–379.
Gibson MJ, Glasser NF, Quincey DJ, et al. (2017) Temporal variations in supraglacial debris distribution on Baltoro Glacier, Karakoram between 2001 and 2012. Geomorphology 295: 572–585. https://doi.org/10.1016/j.geomorph.2017.08.012
Gisin H (1960) Springtail fauna of Europe (Collembolenfauna Europas), 1st ed. Geneva: Museum D’Histoire Naturelle. (In German).
Gobbi M, Bernardi FD, Pelfini M, et al. (2006) Epigean Arthropod Succession along a 154-year Glacier Foreland Chronosequence in the Forni Valley (Central Italian Alps). Arct Antarct Alp Res 38: 357–362. https://doi.org/10.1657/1523-0430(2006)38[357:EASAAY]2.0.CO;2
Gobbi M, Rossaro B, Vater A, et al. (2007) Environmental features influencing Carabid beetle (Coleoptera) assemblages along a recently deglaciated area in the Alpine region. Ecol Entomol 32: 682–689. https://doi.org/10.1111/j.1365-2311.2007.00912.x
Gobbi M, Caccianiga M, Cerabolini BEL, et al. (2010) Plant Adaptative Responses during Primary Succession Are Associated with Functional Adaptations in Ground Beetles on Recently Deglaciated Terrain. Community Ecol 11: 223–231.
Gobbi M, Isaia M, De Bernardi F (2011) Arthropod colonisation of a debris-covered glacier. The Holocene 21: 343–349. https://doi.org/10.1177/0959683610374885
Gobbi M, Ballarin F, Brambilla M, et al. (2017) Life in harsh environments: carabid and spider trait types and functional diversity on a debris-covered glacier and along its foreland: Functional traits in harsh environments. Ecol Entomol 42: 838–848. https://doi.org/10.1111/een.12456
Gobbi M (2020) Global warning: challenges, threats and opportunities for ground beetles (Coleoptera: Carabidae) in high altitude habitats. Acta Zool Acad Sci Hung 66: 5–20. https://doi.org/10.17109/AZH.66.Suppl.5.2020
Gobbi M, Lencioni V (2021) Glacial Biodiversity: Lessons from Ground-dwelling and Aquatic Insects, in: Kanao, M., Godone, D., Dematteis, N. (Eds.), Glaciers and the Polar Environment. IntechOpen. https://doi.org/10.5772/intechopen.92826
Hågvar S, Gobbi M, Kaufmann R, et al. (2020) Ecosystem Birth near Melting Glaciers: A Review on the Pioneer Role of Ground-Dwelling Arthropods. Insects 11, 644. https://doi.org/10.3390/insects11090644
Hammer Ø (1999–2021) PAST: PALeontological STatistics, Version 4.05. Reference manual. 284 pp.
Hammer Ø, Harper DAT, Ryan PD 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 9.
Hannss C (1970) The southernmost Alpine glaciers: observations about glacier morphology in the Maritime Alps, Italian slope (Les glaciers les plus méridionaux des Alpes: Observations de morphologie glaciaire dans les Alpes maritimes, versant italien.) Rev Géographie Alp 58: 619–648. https://doi.org/10.3406/rga.1970.3506 (In French)
Harry I, Drees C, Höfer H, et al. (2011). When to sample in an inaccessible landscape: a case study with carabids from the Allgäu (northern Alps) (Coleoptera, Carabidae) 17.
Holten JI (2003) Altitudinal ranges and spatial patterns of alpine plants in Northern Europe., in: In: Nagy L, Grabherr G, Körner C, Thompson DBA (Eds) Alpine Biodiversity in Europe. Ecological Studies (Analysis and Synthesis). Springer, Berlin, pp. 173–184.
Isaia M, Pantini P, Beikes S et al. (2007) Census of spiders (Arachnida, Araneae) of Piedmont and Lombardy (Catalogo ragionato dei ragni (Arachnida, Araneae) del Piemonte e della Lombardia). Assoc. Naturalistica Piemontese, Erscheinungsort nicht ermittelbar. (In Italian)
Isaia M, Mammola S (2018) Vesubia jugorum. The IUCN Red List of Threatened Species 2018: e.T98700253A98700319.
Jong, Y, et al. (2014) Fauna Europaea - all European animal species on the web. Biodivers. Data J. 2. https://doi.org/10.3897/BDJ.2.e4034
Jordana R (2012) Capbrynae & Entomobryni, Synopses on Palaearctic Collembola. Senckenberg Museum of Natural History Görlitz.
Kaufmann R (2001) Invertebrate Succession on an Alpine Glacier Foreland. Ecology 82: 2261–2278.
Kaufmann R, Fuchs M, Gosterxeier N (2002a) The Soil Fauna of an Alpine Glacier Foreland: Colonization and Succession. Arct Antarct Alp Res 34: 242–250.
Kaufmann R, Juen A (2002b) Habitat use and niche segregation of the genus Nebria (Coleoptera: Carabidae) in the Austrian Alps. Bull Société Entomol Suisse 74: 237–254.
Khedim N, Cécillon L, Poulenard, et al. (2021) Topsoil organic matter build-up in glacier forelands around the world. Glob Change Biol 27: 1662–1677. https://doi.org/10.1111/gcb.15496
Kreyszig E (1979) Advanced Engineering Mathematics, 4th ed. Wiley.
Landolt E, Bäumler A, Erhardt O, et al. (2010) Flora Indicativa, Ecological Indicator Values and Biological Attributes of the Flora of Switzerland and the Alps. Editions Conservatoire Et Jardin Bot de la Ville de Genève, Genève.
Legendre P, Legendre L (1998) Numerical Ecology, 2nd ed. Elsevier Science.
Lencioni V, Gobbi M (2021) Monitoring and conservation of cryophilous biodiversity: concerns when working with insect populations in vanishing glacial habitats. Insect Conserv Divers 14(6): 723–729. https://doi.org/10.1111/icad.12522
Mammola S, Milano F, Cardoso P, et al. (2016) Species conservation profile of the alpine stenoendemic spider Vesubia jugorum (Araneae, Lycosidae) from the Maritime Alps. Biodivers. Data J. 4, e10527. https://doi.org/10.3897/BDJ.4.e10527
Marcante S, Schwienbacher E, Erschbamer E (2009) Genesis of a Soil Seed Bank on a Primary Succession in the Central Alps. Flora 204: 434–444.
Mateos E (2012) The European Lepidocyrtus lanuginosus group (Collembola: Entomobryidae), definition and description of a new species from Spain. Zootaxa 3570: 69. https://doi.org/10.11646/zootaxa.3570.1.5
Matthews JA (1992) The ecology of recently deglaciated terrain: A geoecological approach to glacier forelands and primary succession. Cambridge University Press, Cambridge.
Matthews JA, Hill JL, Winkler S, Owen G, Vater AE (2018) Autosuccession in alpine vegetation: Testing the concept on an altitudinal bioclimatic gradient, Jotunheimen, southern Norway. Catena 170: 169–182. https://doi.org/10.1016/j.catena.2018.06.012
Medail F, Quezel P (1999) Biodiversity Hotspots in the Mediterranean Basin: Setting Global Conservation Priorities. Conserv Biol 13: 1510–1513. https://doi.org/10.1046/j.1523-1739.1999.98467.x
Mihalcea C, Mayer C, Diolaiuti G, et al. (2008) Spatial distribution of debris thickness and melting from remote-sensing and meteorological data, at debris-covered Baltoro glacier, Karakoram, Pakistan. Ann Glaciol 48: 49–57. https://doi.org/10.3189/172756408784700680
Moret P., Barragán Á, Moreno E, et al. (2020) When the Ice Has Gone: Colonisation of Equatorial Glacier Forelands by Ground Beetles (Coleoptera: Carabidae). Neotrop Entomol 49: 213–226. https://doi.org/10.1007/s13744-019-00753-x
Mori AS, Osono T, Uchida M, et al. (2008) Changes in the structure and heterogeneity of vegetation and microsite environments with the chronosequence of primary succession on a glacier foreland in Ellesmere Island, high arctic Canada. Ecol Res 23: 363–370. https://doi.org/10.1007/s11284-007-0388-6
Nakawo M, Rana B (1999) Estimate of Ablation Rate of Glacier Ice under a Supraglacial Debris Layer. Geografiska Ann 81: 695–701.
Nayrolles P, Lienhard C (1990) Description of a new species of Prorastiopes in Switzerland) (Description d’une nouvelle espèce de Prorastriopes de Suisse (Collembola Symphypleona)). Rev Suisse Zool 97: 623–628. (In French)
Oerlemans J (2005) Extracting a Climate Signal from 169 Glacier Records. Science 308: 675–677. https://doi.org/10.1126/science.1107046
Pantini P, Isaia M (2019) Araneae.it: the online Catalog of Italian spiders with addenda on other Arachnid Orders occurring in Italy (Arachnida: Araneae, Opiliones, Palpigradi, Pseudoscorpionida, Scorpiones, Solifugae). Fragm Entomol 51: 127–152.
Paul F, Kääb A, Haeberli W (2007) Recent glacier changes in the Alps observed by satellite: Consequences for future monitoring strategies. Glob Planet Change 56: 111–122. https://doi.org/10.1016/j.gloplacha.2006.07.007
Paul F, Bolch T, Kääb A, et al. (2015) The glaciers climate change initiative: Methods for creating glacier area, elevation change and velocity products. Remote Sens Environ 162: 408–426. https://doi.org/10.1016/j.rse.2013.07.043
Pesarini C, Monzini V (2010) Insects of Italian Fauna. Carabid beetles I (Insetti della Fauna Italiana Coleotteri Carabidi (I).) Natura Rivista Sci Nat 100: 152. (In Italian)
Pesarini C, Monzini V (2011) Insects of Italian Fauna. Carabid beetles II (Insetti della Fauna Italiana Coleotteri Carabidi (II)). Soc Ital Sci Nat 101: 144. (In Italian)
Piana F, Fioraso G, Irace A, et al. (2017) Geology of Piemonte region (NW Italy, Alps-Apennines interference zone). Journal Map13: 395–405. https://doi.org/10.1080/17445647.2017.1316218
Pignatti S (2017) Flora of Italy (Flora d’Italia), 2°. ed. Edagricole, Milano. (In Italian)
Podani J, Csányi B (2010) Detecting indicator species: Some extensions of the IndVal measure. Ecol Indic 10: 1119–1124. https://doi.org/10.1016/j.ecolind.2010.03.010
Potapov M (2001) Isotomidae, Synopses on Palaearctic Collembola. Senckenberg Museum of Natural History Görlitz.
Rapetti F, Vittorini S (1992) Some aspects of the climate of Gesso Valley (Maritime Alps) in relation to the occurrence of some small glaciers (Aspetti del Clima del bacino del Gesso (Alpi Marittime) in relazione alla presenza di alcuni piccoli ghiacciai.) Geogr Fis Din Quat 15: 149–158. (In Italian)
Roberts MJ (1995) Spiders of Britain and Northern Europe, Collins Field Guide.
Roe GH, Baker MB, Herla F (2017) Centennial glacier retreat as categorical evidence of regional climate change. Nat Geosci 10: 95–99. https://doi.org/10.1038/ngeo2863
Rolland C (2003) Spatial and Seasonal Variations of Air Temperature Lapse Rates in Alpine Regions. J Clim 16: 1032–1046.
Rosero P, Crespo-Pérez V, Espinosa R, et al. (2021) Multitaxa colonisation along the foreland of a vanishing equatorial glacier. Ecography 44: 1010–1021. https://doi.org/10.1111/ecog.05478
Rusek J (2001) Microhabitats of Collembola (Insecta: Entognatha) in beech and spruce forests and their influence on biodiversity. Eur J Soil Biol 37: 237–244. https://doi.org/10.1016/S1164-5563(01)01090-1
Schauwecker S, Rohrer M, Huggel C, et al. (2015) Remotely sensed debris thickness mapping of Bara Shigri Glacier, Indian Himalaya. J Glaciol 61: 675–688. https://doi.org/10.3189/2015JoG14J102
Schonswetter P, Stehlik I, Holderegger R, et al. (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14: 3547–3555. https://doi.org/10.1111/j.1365-294X.2005.02683.x
Smiraglia C, Diolaiuti G (2015) New census of Italian glaciers (Il Nuovo Catasto dei Ghiacciai Italiani.) Ev-K2-CNR Ed., Bergamo. (In Italian).
Tampucci D, Gobbi M, Boracchi P, et al. (2015) Plant and arthropod colonisation of a glacier foreland in a peripheral mountain range. Biodiversity 16: 213–223. https://doi.org/10.1080/14888386.2015.1117990
Thaler K (1988) Areal forms in the nival spider fauna of the Eastern Alps (Arealformen in der nivalen Spinnenfauna der Ostalpen (Arachnida, Aranei). Zool Anz 220: 233–244. (In German)
Thibaud JM, Schulz HJ, da Gama Assalino MM (2004) Hypogastruridae, Synopses on Palaearctic Collembola. Senckenberg Museum of Natural History Görlitz.
Valle B, Ambrosini R, Caccianiga M, et al. (2020) Ecology of the cold-adapted species Nebria germari (Coleoptera: Carabidae): the role of supraglacial stony debris as refugium during the current interglacial period. Acta Zool Acad Sci Hung 66: 199–220. https://doi.org/10.17109/AZH.66.Suppl.199.2020
Valle B, Cucini C, Nardi F, et al. (2021) Desoria calderonis sp. nov., a new species of alpine cryophilic springtail (Collembola: Isotomidae) from the Apennines (Italy), with phylogenetic and ecological considerations. European Journal of Taxonomy, 787(1): 32–52. https://doi.org/10.5852/ejt.2021.787.1599
Valle B, Di Musciano M, Gobbi M, et al. (2022) Biodiversity and ecology of plants and arthropods on the last preserved glacier of the Apennines mountain chain (Italy). The Holocene. 32(8): 853–865. https://doi.org/10.1177/09596836221096292
Vater AE, Matthews JA (2013) Testing the ‘addition and persistence model’ of invertebrate succession in a subalpine glacier-foreland chronosequence: Fåbergstølsbreen, southern Norway. The Holocene 23: 1151–1162. https://doi.org/10.1177/0959683613483623
Vater AE, Matthews JA (2015) Succession of pitfall-trapped insects and arachnids on eight Norwegian glacier forelands along an altitudinal gradient: Patterns and models. The Holocene 25: 108–129. https://doi.org/10.1177/0959683614556374
Villemant C, Daugeron C, Gargominy O, et al. (2015) The Mercantour/Alpi Marittime All Taxa Biodiversity Inventory (ATBI): achievements and prospects. Zoosystema 37: 667–679. https://doi.org/10.5252/z2015n4a10
Walker DA, Epstein HE, Gould WA, et al. (2004) Frost-boil ecosystems: complex interactions between landforms, soils, vegetation and climate. Permafr Periglac Process 15: 171–188. https://doi.org/10.1002/ppp.487
Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21: 213–251. https://doi.org/10.2307/1218190
Widenfalk LA, Malmström A, Berg MP, et al. (2016 Small-scale Collembola community composition in a pine forest soil - Overdispersion in functional traits indicates the importance of species interactions. Soil Biol Biochem 103: 52–62. https://doi.org/10.1016/j.soilbio.2016.08.006
Zeleny D (2022) Analysis of community ecology data in R. Ordination analysis. Available online at: https://www.davidzeleny.net/anadatr/doku.php/en:ordination (Accessed on June 2022)
The research was funded by Ente di Gestione delle Aree protette delle Alpi Marittime (Managing Body of protected areas of Maritime Alps) for the research project “Monitoraggio della vegetazione periglaciale dei ghiacciai Clapier e Peirabroc (Alpi Marittime)”, (Monitoring of proglacial vegetation of Clapier and Peirabrocn glaciers (Maritime Alps)) within the project ALCOTRA n. 1711 CClimaTT.
Funding note: Open access funding provided by Università degli Studi di Milano within the CRUI-CARE Agreement.
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Valle, B., Gobbi, M., Tognetti, M. et al. Glacial biodiversity of the southernmost glaciers of the European Alps (Clapier and Peirabroc, Italy). J. Mt. Sci. 19, 2139–2159 (2022). https://doi.org/10.1007/s11629-022-7331-8
- Arthropod communities
- Cold-adapted species
- Glacier forelands
- Plant communities
- Primary succession