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Dispersal patterns of meiospores shape population spatial structure of saxicolous lichens

Published online by Cambridge University Press:  24 July 2017

M. MORANDO ,
S. E. FAVERO-LONGO ,
M. CARRER ,
E. MATTEUCCI ,
J. NASCIMBENE ,
S. SANDRONE ,
L. APPOLONIA  and
R. PIERVITTORI
M. MORANDO
Affiliation:
Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Viale Mattioli 25, 10125 Torino, Italy.
S. E. FAVERO-LONGO*
Affiliation:
Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Viale Mattioli 25, 10125 Torino, Italy.
M. CARRER
Affiliation:
Dipartimento Territorio e Sistemi Agro-Forestali, Università degli Studi di Padova, Viale dell’Università 16, 35020 Legnaro (PD), Italy
E. MATTEUCCI
Affiliation:
Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Viale Mattioli 25, 10125 Torino, Italy.
J. NASCIMBENE
Affiliation:
Dipartimento di Biologia, Università degli Studi di Padova, Via U. Bassi 58/ B, 35121 Padova, Italy
S. SANDRONE
Affiliation:
Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Viale Mattioli 25, 10125 Torino, Italy.
L. APPOLONIA
Affiliation:
Laboratorio Analisi Scientifica, Direzione Ricerca e Progetti Cofinanziati, Soprintendenza per i Beni e le Attività Culturali, Regione Autonoma Valle d’Aosta, Piazza Narbonne 3, 11100 Aosta, Italy
R. PIERVITTORI
Affiliation:
Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Viale Mattioli 25, 10125 Torino, Italy.
*
Email: sergio.favero@unito.it
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Abstract

Relationships between reproductive strategies and population spatial structure have often been suggested for lichens, but there is a lack of supporting aerobiological data. For the first time, this study couples aerobiological investigations on meiospore dispersal by Caloplaca crenulatella (Nyl.) H. Olivier and Rhizocarpon geographicum (L.) DC. with analysis of local spatial patterns of thalli of both species. During a two-year monitoring period carried out on the walls of a medieval castle in NW Italy, a total of 169 polar diblastic spores, 20% of which were morphologically attributable to C. crenulatella, was detected in the mycoareosol, while muriform spores of R. geographicum were never found. Laboratory experiments confirmed that different dispersal patterns characterize the two species, the meiospores of R. geographicum being poorly discharged and only recovered at a short distance from thalli, whereas those of C. crenulatella were more abundantly discharged, suspended and better dispersed by a moderate air flow. This difference was reflected on the castle walls by the random spatial pattern of C. crenulatella, while R. geographicum showed a clustered distribution. Different discharge rates and take-off limitations, possibly related to size differences between the spores, are not sufficient to explain the different colonization patterns and dynamics of the two species. Additional intrinsic and extrinsic factors are likely to drive their dispersal and establishment success. Nevertheless, information on the relationships between different dispersal patterns of the species and the local spatial structure of their populations might help to predict the recovery potential of lichen species exposed to habitat loss or disturbance, or encrusting monument surfaces.

Keywords

aerobiologyCaloplaca crenulatellaRhizocarpon geographicumstone cultural heritagesubstratum preference
Type
Articles
Information
The Lichenologist , Volume 49 , Issue 4 , July 2017 , pp. 397 - 413
Copyright
© British Lichen Society, 2017 

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References

Aakala, T., Fraver, S., Palik, B. J. & D’Amato, A. W. (2012) Spatially random mortality in old-growth red pine forests of northern Minnesota. Canadian Journal of Forest Research 42: 899–907.Google Scholar
Arbia, G. (2001) The role of spatial effects in the empirical analysis of regional concentration. Journal of Geographical Systems 3: 271–281.CrossRefGoogle Scholar
Armstrong, R. A. (1981) Field experiments on the dispersal, establishment and colonization of lichens on a slate rock surface. Environmental and Experimental Botany 21: 115–120.Google Scholar
Armstrong, R. & Bradwell, T. (2010) Growth of crustose lichens: a review. Geografiska Annaler: Series A, Physical Geography 92: 3–17.Google Scholar
Bailey, R. H. (1976) Ecological aspects of dispersal and establishment in lichens. In Lichenology: Progress and Problems (D. H. Brown, D. L. Hawksworth & R. H. Bailey, eds): 215–247. London: Academic Press.Google Scholar
Bailey, R. H. & Garrett, R. M. (1968) Studies on the discharge of ascospores from lichen apothecia. Lichenologist 4: 57–65.Google Scholar
Belinchón, R., Yahr, R. & Ellis, C. J. (2015) Interactions among species with contrasting dispersal modes explain distributions for epiphytic lichens. Ecography 38: 762–768.Google Scholar
Bellemère, A. & Letrouit-Galinou, M. A. (1988) Asci, ascospores, and ascomata. In Handbook of Lichenology. Vol. I (M. Galun, ed.): 161–179. Boca Raton: CRC Press.Google Scholar
Boch, S., Prati, D., Werth, S., Rüetschi, J. & Fischer, M. (2011) Lichen endozoochory by snails. PLoS ONE 6: e18770.Google Scholar
Brodo, I. M. (1973) Substrate ecology. In The Lichens (V. Ahmadjian & M. E. Hale, eds): 401–441. New York: Academic Press.Google Scholar
Clayden, S. R. (1997) Seasonal variation in ascospore discharge by Rhizocarpon lecanorinum . Lichenologist 29: 495–499.CrossRefGoogle Scholar
Crittenden, P. D., David, J. C., Hawksworth, D. L. & Campbell, F. S. (1995) Attempted isolation and success in the culturing of a broad spectrum of lichen‐forming and lichenicolous fungi. New Phytologist 130: 267–297.Google Scholar
De Nuntiis, P., Maggi, O., Mandrioli, P., Ranalli, G. & Sorlini, C. (2003) Monitoring the biological aerosol. In Cultural Heritage and Aerobiology (P. Madrioli, G. Caneva & C. Sabbioni, eds): 107–144. Dordrecht: Kluwer Academic Publishers.Google Scholar
Descamps, I., Harion, J. L. & Baudoin, B. (2005) Taking-off model of particles with a wide size distribution. Chemical Engineering and Processing 44: 159–166.Google Scholar
Ellis, C. J. (2012) Lichen epiphyte diversity: a species, community and trait-based review. Perspectives in Plant Ecology, Evolution and Systematics 14: 131–152.Google Scholar
Ellis, C. J. & Coppins, B. J. (2007) Reproductive strategy and the compositional dynamics of crustose lichen communities on aspen (Populus tremula L.) in Scotland. Lichenologist 39: 377–391.Google Scholar
Favero-Longo, S. E., Sandrone, S., Matteucci, E., Appolonia, L. & Piervittori, R. (2014) Spores of lichen-forming fungi in the mycoaerosol and their relationships with climate factors. Science of the Total Environment 466: 26–33.CrossRefGoogle ScholarPubMed
Garrett, R. M. (1971) Studies on some aspects of ascospore liberation and dispersal in lichens. Lichenologist 5: 33–44.Google Scholar
Gazzano, C., Favero-Longo, S. E., Matteucci, E., Roccardi, A. & Piervittori, R. (2009) Index of Lichen Potential Biodeteriogenic Activity (LPBA): a tentative tool to evaluate the lichen impact on stonework. International Biodeterioration and Biodegradation 63: 836–843.Google Scholar
Getis, A. & Ord, J. K. (1992) The analysis of spatial association by use of distance statistics. Geographical Analysis 24: 189–199.Google Scholar
Getis, A. & Ord, J. K. (1996) Local spatial statistics: an overview. In Spatial Analysis: Modelling in a GIS Environment (P. Longley & M. Batty, eds): 161–177. New York: Wiley.Google Scholar
Giordani, P. & Brunialti, G. (2015) Sampling and interpreting lichen diversity data for biomonitoring purposes. In Recent Advances in Lichenology. Modern Methods and Approaches in Biomonitoring and Bioprospection, Volume 1 (D. K. Upreti, P. K. Divakar, V. Shukla & R. Bajpai, eds): 19–46. New Delhi: Springer India.CrossRefGoogle Scholar
Giordani, P., Incerti, G., Rizzi, G., Rellini, I., Nimis, P. L. & 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.Google Scholar
Gjerde, I., Blom, H. H., Heegaard, E. & Sætersdal, M. (2015) Lichen colonization patterns show minor effects of dispersal distance at landscape scale. Ecography 38: 939–948.Google Scholar
Hedenås, H., Bolyukh, V. O. & Jonsson, B. G. (2003) Spatial distribution of epiphytes on Populus tremula in relation to dispersal mode. Journal of Vegetation Science 14: 233–242.Google Scholar
Jettestuen, E., Nermoen, A., Hestmark, G., Timdal, E. & Mathiesen, J. (2010) Competition on the rocks: community growth and tessellation. PloS ONE 5: e12820.Google Scholar
Johansson, V., Ranius, T. & Snäll, T. (2012) Epiphyte metapopulation dynamics are explained by species traits, connectivity, and patch dynamics. Ecology 93: 235–241.Google Scholar
John, E. & Dale, M. R. T. (1991) Determinants of spatial pattern in saxicolous lichen communities. Lichenologist 23: 227–236.Google Scholar
Kuparinen, A., Markkanen, T., Riikonen, H. & Vesala, T. (2007) Modeling air-mediated dispersal of spores, pollen and seeds in forested areas. Ecological Modelling 208: 177–188.Google Scholar
Lacey, J. (1996) Spore dispersal – its role in ecology and disease: the British contribution to fungal aerobiology. Mycological Research 100: 641–660.CrossRefGoogle Scholar
Lawrey, J. D. (1984) Biology of Lichenized Fungi. New York: Praeger Publishers.Google Scholar
Lawrey, J. D. (1991) Biotic interactions in lichen community development: a review. Lichenologist 23: 205–214.Google Scholar
Leavitt, S. D. & Lumbsch, H. T. (2016) Ecological biogeography of lichen-forming fungi. In The Mycota: Environmental and Microbial Relationships IV, 3rd edition (I. S. Druzhinina & C. P. Kubicek, eds): 15–37. Cham: Springer International Publishing Switzerland.Google Scholar
Leger, E. A. & Forister, M. L. (2009) Colonization, abundance, and geographic range size of gravestone lichens. Basic and Applied Ecology 10: 279–287.Google Scholar
Loso, M. G. & Doak, D. F. (2006) The biology behind lichenometric dating curves. Oecologia 147: 223–229.Google Scholar
Magyar, D., Vass, M. & Li, D. W. (2016) Dispersal strategies of microfungi. In Biology of Microfungi (D. W. Li, ed.): 315–371. Cham: Springer International Publishing Switzerland.Google Scholar
Marshall, W. A. (1996) Aerial dispersal of lichen soredia in the maritime Antarctic. New Phytologist 134: 523–530.Google Scholar
McIlroy de la Rosa, J. P. M., Porcel, M. C. & Warke, P. A. (2013) Mapping stone surface temperature fluctuations: implications for lichen distribution and biomodification on historic stone surfaces. Journal of Cultural Heritage 14: 346–353.Google Scholar
Moran, P. A. P. (1950) Notes on continuous stochastic phenomena. Biometrika 37: 17–33.Google Scholar
Nascimbene, J. & Marini, L. (2015) Epiphytic lichen diversity along elevational gradients: biological traits reveal a complex response to water and energy. Journal of Biogeography 42: 1222–1232.Google Scholar
Noblin, X., Yang, S. & Dumais, J. (2009) Surface tension propulsion of fungal spores. Journal of Experimental Biology 212: 2835–2843.Google Scholar
Piervittori, R., Laccisaglia, A., Appolonia, L. & Gallo, L. M. (1991) Aspetti floristico-vegetazionali e metodologici relativi ai licheni su materiali lapidei in Valle d’Aosta. Revue Valdôtaine d’Histoire Naturelle 45: 53–86.Google Scholar
Prieto, B., Rivas, T. & Silva, B. (1999) Environmental factors affecting the distribution of lichens on granitic monuments in the Iberian Peninsula. Lichenologist 31: 291–305.Google Scholar
Pyatt, F. B. (1973) Lichen propagules. In The Lichens (V. Ahmadjian & M. E. Hale, eds): 117–145. New York: Academic Press.Google Scholar
Raventós, J., Wiegand, T. & De Luis, M. (2010) Evidence for the spatial segregation hypothesis: a test with nine-year survivorship data in a Mediterranean shrubland. Ecology 91: 2110–2120.CrossRefGoogle Scholar
Sanders, W. B. (2014) Complete life cycle of the lichen fungus Calopadia puiggarii (Pilocarpaceae, Ascomycetes) documented in situ: propagule dispersal, establishment of symbiosis, thallus development, and formation of sexual and asexual reproductive structures. American Journal of Botany 101: 1836–1848.Google Scholar
Sartorio, G. (2012) Il cantiere della conoscenza del castello di Graines: elementi di storia e di archeologia. In Colloque de Clôture du Projet Anciens Vestiges en Ruine (AVER), 29 Novembre–1 Décembre, 2012, Aoste, Italie, pp. 33–56.Google Scholar
Sawada, M. (1999) ROOKCASE: an Excel 97/Visual Basic (VB) add-in for exploring global and local spatial autocorrelation. Bulletin of the Ecological Society of America 80: 231–234.Google Scholar
Schei, F. H., Blom, H. H., Gjerde, I., Grytnes, J. A., Heegaard, E. & Sætersdal, M. (2012) Fine‐scale distribution and abundance of epiphytic lichens: environmental filtering or local dispersal dynamics? Journal of Vegetation Science 23: 459–470.Google Scholar
Scheidegger, C. & Werth, S. (2009) Conservation strategies for lichens: insights from population biology. Fungal Biology Reviews 23: 55–66.Google Scholar
Seaward, M. R. D. (1977) Lichen Ecology. London: Academic Press.Google Scholar
Seaward, M. R. D. (2015) Lichens as agents of biodeterioration. In Recent Advances in Lichenology. Modern Methods and Approaches in Biomonitoring and Bioprospection, Volume 1 (D. K. Upreti, P. K. Divakar, V. Shukla & R. Bajpai, eds): 189–211. New Delhi: Springer India.Google Scholar
Sergi, A. (2012) Interventi conservativi al castello di Graines e alla casaforte di Saint-Marcel. Riflessioni su alcuni principi del restauro monumentale applicato. La metodologia del progetto AVER alla luce dei risultati sul campo. In Colloque de Clôture du Projet Anciens Vestiges en Ruine (AVER), 29 Novembre–1 Décembre, 2012, Aoste, Italie, pp. 185–224.Google Scholar
Smith, P. L. (2014) Lichen translocation with reference to species conservation and habitat restoration. Symbiosis 62: 17–28.Google Scholar
Spitale, D. & Nascimbene, J. (2012) Spatial structure, rock type, and local environmental conditions drive moss and lichen distribution on calcareous boulders. Ecological Research 27: 633–638.Google Scholar
Travaglini, A., Albertini, R. & Zieger, E. (2009) Manuale di Gestione e Qualità della Rete Italiana di Monitoraggio in Aerobiologia R.I.M.A. Ozzano dell’Emilia: L.E.G.O. s.p.a. Calderini.Google Scholar
Verger, J. P. (1992) Vegetation and soils in the Valle d’Aosta (Italy). In The Vegetation of Ultramafic (Serpentine) Soils (A. J. M. Baker, J. Proctor & R. D. Reeves, eds): 175–195. Andover: Intercept.Google Scholar
Werth, S., Cheenacharoen, S. & Scheidegger, C. (2014) Propagule size is not a good predictor for regional population subdivision or fine-scale spatial structure in lichenized fungi. Fungal Biology 118: 126–138.Google Scholar
Wiegand, T. & Moloney, K. A. (2004) Rings, circles, and null-models for point pattern analysis in ecology. Oikos 104: 209–229.Google Scholar
Wiegand, T. & Moloney, K. A. (2013) Handbook of Spatial Point-Pattern Analysis in Ecology. Boca Raton: CRC Press, Taylor & Francis Group.Google Scholar
Wiegand, T., Gunatilleke, S., Gunatilleke, N. & Okuda, T. (2007) Analyzing the spatial structure of a Sri Lankan tree species with multiple scales of clustering. Ecology 88: 3088–3102.Google Scholar
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