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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Metals and secondary metabolites in saxicolous lichen communities on ultramafic and non-ultramafic rocks of the Western Italian Alps

Sergio E. Favero-Longo A D , Enrica Matteucci A , Mariagrazia Morando A , Franco Rolfo B , Tanner B. Harris C and Rosanna Piervittori A
+ Author Affiliations
- Author Affiliations

A Department of Life Sciences and Systems Biology, University of Torino, Viale Mattioli 25, 10125, Torino, Italy.

B Department of Earth Sciences, University of Torino, Via Valperga Caluso 35, 10125, Torino, Italy.

C College of the Atlantic, 105 Eden Street, Bar Harbor, ME 04609, USA.

D Corresponding author. Email: sergio.favero@unito.it

Australian Journal of Botany 63(4) 276-291 https://doi.org/10.1071/BT14256
Submitted: 8 October 2014  Accepted: 12 February 2015   Published: 28 April 2015

Abstract

There is a long history of studies on lichens found in ultramafic habitats, but comparisons between lichen communities on different ultramafic lithologies are scant, and potential metabolic adaptations to the multiple edaphic stresses of ultramafic substrates have been widely neglected. The present work is the first to characterise differences in the abundance and structure of saxicolous lichen communities on different ultramafic lithologies (dunite, lherzolite, and serpentinite), analysed in two areas of the Western Alps (NW Italy). Differences between communities on various ultramafic lithologies were observed, including differences between a mafic control (Mg-Al metagabbro); however, factors other than the substrate were observed to drive more remarkable differences between lichen communities on ultramafics of alpine and pre-alpine areas. XRF analyses demonstrated that the mineral composition of different lithologies is reflected by metal contents in crustose lichens, with weathering processes accounting for relative shifts in elemental abundances between rocks and thalli. A thin layer cromatography screening of lichen secondary metabolites (LSMs), which are thought to regulate metal and pH homeostasis in thalli, revealed lithological vicariance among dominant lichen species with different LSM patterns and intraspecific variability in LSM production associated with differences in lithology and location. In particular, the presence or absence of norstictic acid in species or lineages/individuals on the different lithologies, in relationship to concentrations of Fe, Mg, and Ni in lichen thalli, was recognised as a metabolic adaptation to metal stress. Pull-up tests revealed that physical factors such as a differential surface disaggregation may contribute more towards differences observed in lichen abundance on the different lithologies investigated.

Additional keywords: lichen diversity, metal stress, norstictic acid, SDR analysis, serpentine ecosystem, X-ray fluorescence.


References

Adamo P, Violante P (2000) Weathering of rocks and neogenesis of minerals associated with lichen activity. Applied Clay Science 16, 229–256.
Weathering of rocks and neogenesis of minerals associated with lichen activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVCit7w%3D&md5=60e1e848b2740c7a62d1bba542d5aefbCAS |

Bačkor M, Fahselt D (2004) Using EDX-microanalysis and X-ray mapping to demonstrate metal uptake by lichens. Biologia 59, 39–45.

Bačkor M, Fahselt D (2008) Lichen photobionts and metal toxicity. Symbiosis 46, 1–10.

Bačkor M, Loppi S (2009) Interactions of lichens with heavy metals. Biologia Plantarum 53, 214–222.
Interactions of lichens with heavy metals.Crossref | GoogleScholarGoogle Scholar |

Bačkor M, Péli ER, Vantová I (2011) Copper tolerance in the macrolichens Cladonia furcata and Cladina arbuscula subsp. mitis is constitutive rather than inducible. Chemosphere 85, 106–113.
Copper tolerance in the macrolichens Cladonia furcata and Cladina arbuscula subsp. mitis is constitutive rather than inducible.Crossref | GoogleScholarGoogle Scholar | 21676428PubMed |

Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annual Review of Ecology Evolution and Systematics 36, 243–266.
Evolutionary ecology of plant adaptation to serpentine soils.Crossref | GoogleScholarGoogle Scholar |

Brodo IM (1973) Substrate ecology. In ‘The lichens’. (Eds V Ahmadjian, ME Hale) pp. 401–441 (Academic Press: New York)

D’Amico M, Julitta F, Previtali F, Cantelli D (2008) Podzolization over ophiolitic materials in the western Alps (Natural Park of Mont Avic, Aosta Valley, Italy). Geoderma 146, 129–137.
Podzolization over ophiolitic materials in the western Alps (Natural Park of Mont Avic, Aosta Valley, Italy).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVKqtrc%3D&md5=c6bdddafa4aff29a8527984ff30d60beCAS |

Echevarria G (2014) The availability of nickel in ultramafic soils. In ‘The official programme book of the 8th international congress on serpentine ecology’. p. 37. (ICSE2014: Kota Kinabalu, Malaysia)

Elix JA, Stocker-Wörgötter E (2008) Biochemistry and secondary metabolites. In ‘Lichen biology’. (Ed. TH Nash III) pp. 104–133. (Cambridge University Press: Cambridge)

Elter FM, Piccardo GB, Polino R, Zanetti A, Spagnolo G, Poggi E, Balbi P (2005) Structural and compositional features of the Mt Musinè peridotites (Lanzo Massif, Western Alps, Italy). Ofioliti 30, 161–173.

Favero-Longo SE (2014) Lichens on metal-rich substrates. In ‘Plant ecology and evolution in harsh environments’. (Eds N Rajakaruna, T Harris, R Boyd) pp. 53–76 (Nova Publishers: New York)

Favero-Longo SE, Piervittori R (2009) Measuring biodiversity of saxicolous lichens above timberline with reference to environmental factors: the case-study of a Natura 2000 site of western Alps. Phytocoenologia 39, 51–78.
Measuring biodiversity of saxicolous lichens above timberline with reference to environmental factors: the case-study of a Natura 2000 site of western Alps.Crossref | GoogleScholarGoogle Scholar |

Favero-Longo SE, Isocrono D, Piervittori R (2004) Lichens and ultramafic rocks: a review. Lichenologist (London, England) 36, 391–404.
Lichens and ultramafic rocks: a review.Crossref | GoogleScholarGoogle Scholar |

Favero-Longo SE, Castelli D, Salvadori O, Belluso E, Piervittori R (2005) Pedogenetic action of Lecidea atrobrunnea, Rhizocarpon geographicum gr. and Sporastatia testudinea on serpentinized ultramafic rocks in an alpine environment. International Biodeterioration & Biodegradation 56, 17–27.
Pedogenetic action of Lecidea atrobrunnea, Rhizocarpon geographicum gr. and Sporastatia testudinea on serpentinized ultramafic rocks in an alpine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsVWntrw%3D&md5=26c784208c76600a1a24245566556426CAS |

Favero-Longo SE, Castelli D, Fubini B, Piervittori R (2009) Lichens on asbestos cement roofs: bioweathering and biocovering effects. Journal of Hazardous Materials 162, 1300–1308.
Lichens on asbestos cement roofs: bioweathering and biocovering effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWrsLfL&md5=b7497938cff70f05b1e6e71f9480ba05CAS | 18692312PubMed |

Favero-Longo SE, Turci F, Castelli D, Fubini B, Piervittori R (2013) Lichen deterioration of asbestos and asbestiform minerals of serpentinite rocks in Western Alps. International Biodeterioration & Biodegradation 84, 342–350.
Lichen deterioration of asbestos and asbestiform minerals of serpentinite rocks in Western Alps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSmtrjK&md5=dbbfe6275b71ca026a72feb2f590493bCAS |

Fryday AM (2005) The genus Porpidia in northern and western Europe, with special emphasis on collections from the British Isles. Lichenologist (London, England) 37, 1–35.
The genus Porpidia in northern and western Europe, with special emphasis on collections from the British Isles.Crossref | GoogleScholarGoogle Scholar |

Gallo LM, Piervittori R (1991) La flora lichenica rupicola dei Monti Pelati di Baldissero (Canavese, Piemonte). In ‘I Monti Pelati di Baldissero. Importanza paesistica e scientifica – Congress Proceedings’. (Ed. PM Giachino) pp. 25–31. (Feletto, Torino)

Gilbert OL (1983) The lichens of Rhum. Transactions of the Botanical Society of Edinburgh 44, 139–149.
The lichens of Rhum.Crossref | GoogleScholarGoogle Scholar |

Giordani P, Incerti G, Rizzi G, Rellini I, Nimis PL, Modenesi P (2014) Functional traits of cryptogams in Mediterranean ecosystems are driven by water, light and substrate interactions. Journal of Vegetation Science 25, 778–792.
Functional traits of cryptogams in Mediterranean ecosystems are driven by water, light and substrate interactions.Crossref | GoogleScholarGoogle Scholar |

Harrison S, Rajakaruna N (2011) ‘Serpentine. The evolution and ecology of a model system.’ (University of California Press: Berkeley, CA, USA)

Hauck M, Huneck S, Elix JA, Paul A (2007) Does secondary chemistry enable lichens to grow on iron-rich substrates? Flora 202, 471–478.
Does secondary chemistry enable lichens to grow on iron-rich substrates?Crossref | GoogleScholarGoogle Scholar |

Hauck M, Jürgens S-R, Willenbruch K, Huneck S, Leuschner C (2009) Dissociation and metal-binding characteristics of yellow substances suggest a relationship with site preferences of lichens. Annals of Botany 103, 13–22.
Dissociation and metal-binding characteristics of yellow substances suggest a relationship with site preferences of lichens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislOju7o%3D&md5=611d18fe460ff8dc0fb9e66c7f12da2aCAS | 18977765PubMed |

Hauck M, Jürgens S-R, Leuschner C (2010) Norstictic acid: correlations between its physico-chemical characteristics and ecological preferences of lichens producing this depsidone. Environmental and Experimental Botany 68, 309–313.
Norstictic acid: correlations between its physico-chemical characteristics and ecological preferences of lichens producing this depsidone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1Wlu7s%3D&md5=9ae6482ef78814924230a94682753fbfCAS |

Hauck M, Böning J, Jacob M, Dittrich S, Feussner I, Leuschner C (2013) Lichen substance concentrations in the lichen Hypogymnia physodes are correlated with heavy metal concentrations in the substrate. Environmental and Experimental Botany 85, 58–63.
Lichen substance concentrations in the lichen Hypogymnia physodes are correlated with heavy metal concentrations in the substrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVyqtLnI&md5=bfd82194478ae81672d15b1f8430b0c1CAS |

Hidalgo ME, Fernandez E, Ponce M, Rubio C, Quilhot W (2002) Photophysical, photochemical, and thermodynamic properties of shikimic acid derivatives: calycin and rhizocarpic acid (lichens). Journal of Photochemistry and Photobiology. B, Biology 66, 213–217.
Photophysical, photochemical, and thermodynamic properties of shikimic acid derivatives: calycin and rhizocarpic acid (lichens).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivValtrg%3D&md5=e88ab3897d0cd3add035edc662b9f17bCAS | 11960732PubMed |

Huneck S, Yoshimura I (1996) ‘Identification of lichen substances.’ (Springer: Berlin)

Kantvilas G, Elix JA (2013) The lichen genus Lecidella (Lecanoraceae), with special reference to the Tasmanian species. Muelleria 31, 31–47.

Kay K, Ward KL, Watt LR, Schemske DW (2011) Plant speciation. In ‘Serpentine. The evolution and ecology of a model system’. (Eds S Harrison, N Rajakaruna) pp. 71–95. (University of California Press: Berkeley, CA, USA)

Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-off tolerance and adaptation to serpentine soils: from species to ecosystem level. Biological Reviews of the Cambridge Philosophical Society 83, 495–508.

Kierczak J, Neel C, Bril H, Puziewicz J (2007) Effect of mineralogy and pedoclimatic variations on Ni and Cr distribution in serpentine soils under temperate climate. Geoderma 142, 165–177.
Effect of mineralogy and pedoclimatic variations on Ni and Cr distribution in serpentine soils under temperate climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFels7rO&md5=b24d0d1edaa415b7401fe645429d6a70CAS |

Leuckert C, Knoph J-G (1992) European taxa of saxicolous Lecidella containing chloroxanthones: identification of patterns using thin layer chromatography. Lichenologist (London, England) 24, 383–397.

Nash TH, III (2008) ‘Lichen Biology’. 2nd edition. (Cambridge University Press: Cambridge)

Nimis PL, Martellos S (2008) ITALIC – The information system in Italian lichens. Ver. 4.0. University of Trieste, Dept. of Biology, IN4.0/1. Available at http://dbios.univ.trieste.it. [Verified 16 September 2014].

Nordin A, Savić S, Tibell L (2010) Phylogeny and taxonomy of Aspicilia and Megasporaceae. Mycologia 102, 1339–1349.
Phylogeny and taxonomy of Aspicilia and Megasporaceae.Crossref | GoogleScholarGoogle Scholar | 20943564PubMed |

O’Hanley D (1996) Serpentinites. Records of tectonics and petrological history.’ In ‘Oxford monographs on geology and geophysics 34’. pp. 277. (Oxford University Press: Oxford)

Orange A, James PW, White FJ (2010) ‘Microchemical methods for the identification of lichens.’ (British Lichen Society: London)

Parrot D, Jan S, Baert N, Guyot S, Tomasi S (2013) Comparative metabolite profiling and chemical study of Ramalina siliquosa complex using LC–ESI-MS/MS approach. Phytochemistry 89, 114–124.
Comparative metabolite profiling and chemical study of Ramalina siliquosa complex using LC–ESI-MS/MS approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFCgur8%3D&md5=b97eccf07d1dd46b7e2034f207461723CAS | 23489575PubMed |

Paukov AG (2009) The lichen flora of serpentine outcrops in the Middle Urals of Russia. Northeastern Naturalist 16, 341–350.

Pawlik-Skowrońska B, Bačkor M (2011) Zn/Pb-tolerant lichens with higher content of secondary metabolites produce less phytochelatins than specimens living in unpolluted habitats. Environmental and Experimental Botany 72, 64–70.
Zn/Pb-tolerant lichens with higher content of secondary metabolites produce less phytochelatins than specimens living in unpolluted habitats.Crossref | GoogleScholarGoogle Scholar |

Podani J, Schmera D (2011) A new conceptual and methodological framework for exploring and explaining pattern in presence–absence data. Oikos 120, 1625–1638.
A new conceptual and methodological framework for exploring and explaining pattern in presence–absence data.Crossref | GoogleScholarGoogle Scholar |

Purvis OW, Pawlik-Skowrońska B (2008). Lichens and metals. In ‘Stress in yeasts and filamentous fungi’, (Eds SV Avery, M Stratford, P van West) pp. 175–200. (Elsevier: Amsterdam)

Rajakaruna N, Knudsen K, Fryday AM, O’Dell RE, Pope N, Olday FC, Woolhouse S (2012) Investigation of the importance of rock chemistry for saxicolous lichen communities of the New Idria serpentinite mass, San Benito County, California, USA. Lichenologist (London, England) 44, 695–714.
Investigation of the importance of rock chemistry for saxicolous lichen communities of the New Idria serpentinite mass, San Benito County, California, USA.Crossref | GoogleScholarGoogle Scholar |

Roberts BA, Proctor J (1992) ‘The ecology of areas with serpentinized rocks. A world view.’ (Kluwer: Dordrecht, The Netherlands)

Rolfo F, Balestro G, Borghi A, Castelli D, Ferrando S, Groppo C, Mosca P, Rossetti P (2015) The Monviso Ophiolite Geopark, a symbol of the Alpine Chain and Geological Heritage in Piemonte, Italy. In ‘Engineering geology for society and territory. Vol. 8’. (Eds G Lollino, D Giordan, C Marunteanu, B Christaras, I Yoshinori, CG Margottini) pp. 239–243. (Springer International Publishing AG: Cham, Switzerland)

Sirois L, Lutzoni F, Grandtner MM (1988) Les lichens sur serpentine et anphibolite du plateau du mont Albert, Gaspésie, Québec. Canadian Journal of Botany 66, 851–862.
Les lichens sur serpentine et anphibolite du plateau du mont Albert, Gaspésie, Québec.Crossref | GoogleScholarGoogle Scholar |

Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (2009) ‘The lichens of Great Britain and Ireland.’ (The British Lichen Society and The Natural History Museum: London)

Spandler C, Pettke T, Rubatto D (2011) Internal and external fluid sources for eclogite-facies veins in the Monviso meta-ophiolite, Western Alps: implications for fluid flow in subduction zones. Journal of Petrology 52, 1207–1236.
Internal and external fluid sources for eclogite-facies veins in the Monviso meta-ophiolite, Western Alps: implications for fluid flow in subduction zones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnslOmsLY%3D&md5=0f16e40a96f466a75de5e979cd94a3b4CAS |

Suza J (1927) Lichenologický ráz západočeských serpentinů. Casopis Moravského. Zemského Musea 25, 251–281.

Ter Braak CJF, Šmilauer P (2002) ‘CANOCO reference manual and Canodraw for Windows user’s guide: software for canonical community ordination (Ver. 4.5).’ (Microcomputer Power: Ithaca, NY, USA)

Ter Braak CJF, Verdonschot PFM (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquatic Sciences 57, 255–289.
Canonical correspondence analysis and related multivariate methods in aquatic ecology.Crossref | GoogleScholarGoogle Scholar |

Vaggelli G, Serra M, Cossio R, Borghi A (2014) A new approach for provenance studies of archaeological finds: inferences from trace elements in carbonate minerals of Alpine white marbles by a bench-to-top μ-XRF spectrometer. International Journal of Mineralogy 2014, 217916
A new approach for provenance studies of archaeological finds: inferences from trace elements in carbonate minerals of Alpine white marbles by a bench-to-top μ-XRF spectrometer.Crossref | GoogleScholarGoogle Scholar |

Wedin M, Westberg M, Crewe AT, Tehler A, Purvis OW (2009) Species delimitation and evolution of metal bioaccumulation in the lichenized Acarospora smaragdula (Ascomycota, Fungi) complex. Cladistics 25, 161–172.
Species delimitation and evolution of metal bioaccumulation in the lichenized Acarospora smaragdula (Ascomycota, Fungi) complex.Crossref | GoogleScholarGoogle Scholar |

Wilson MJ (2004) Weathering of the primary rock-forming minerals: processes, products and rates. Clay Minerals 39, 233–266.
Weathering of the primary rock-forming minerals: processes, products and rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVaqtb3E&md5=f41565381cce841fae3a962a7ea9b17eCAS |

Wirth V (1995) ‘Die Flechten. Baden-Württembergs.’ (Ulmer: Stuttgart, Germany)

Zahlbruckner A (1907) Aufzälung der von Dr. H. Bretzl in Griechenland gesammelten Flechten. Hedwigia 47, 60–65.