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1876 the Reduction of Current Biodiversity Is One of the Major American Journal of Botany 101 ( 11 ): 1876 – 1885 , 2014 . E NVIRONMENTAL FACTORS THAT DRIVE THE DISTRIBUTION AND ABUNDANCE OF A THREATENED CYANOLICHEN IN SOUTHERN EUROPE: A MULTI-SCALE APPROACH 1 S ONIA M ERINERO 2 , M ARTA R UBIO-SALCEDO , G REGORIO A RAGÓN , AND I SABEL M ARTÍNEZ Universidad Rey Juan Carlos, Departamento de Biología y Geología, Área de Biodiversidad y Conservación, C/ Tulipá n s/n E-28933, Madrid, Spain • Premise of the study: High-quality information about threatened species is required to prevent current global biodiversity losses. Lichens are important components of forest biodiversity and help to maintain ecosystem functioning. The epiphytic cya- nolichen Lobarina scrobiculata is red-listed in Europe and North America, but knowledge of its ecology and distribution in Southern Europe is scarce. • Methods: We used a multispatial scale design to investigate the effects of macroclimate, forest structure, tree features, and microhabitat on the occurrence, abundance, spatial distribution, and performance of Lobarina scrobiculata in the Iberian Pen- insula at plot and tree scales. Generalized linear models and mixed models were used for analysis. • Key results: We recorded ca 14 000 individuals of the threatened species Lobarina scrobiculata from 22 populations in the Iberian Peninsula. Our results suggest that L. scrobiculata thrives mainly in oak forests with highly variable annual precipita- tion levels. At the plot scale, the L. scrobiculata abundance increased with annual precipitation and tree density (habitat quan- tity). At the tree scale, our models highlighted the importance of tree size and bark roughness (habitat quality) as the main drivers of species occurrence and abundance. We detected a marked spatial pattern on tree trunks, i.e., L. scrobiculata occurred preferentially on north-facing surfaces and close to the ground where humidity is higher. • Conclusions: By integrating multiscale modeling, we analyzed a unique large dataset and these results are essential for under- standing the ecology of this threatened cyanolichen. There is an urgent need to preserve the forests that this species currently inhabits as well as potential colonization sites. Key words: Atlantic forest; conservation status; epiphytic lichens; Lobaria scrobiculata ; Lobarina scrobiculata ; Mediterra- nean forest; occupation rate; population size; precipitation. The reduction of current biodiversity is one of the major scale, climatic conditions may infl uence the life cycle and per- challenges faced by society in the current century and it is the formance of species, thereby shifting the species habitat quality role of scientists to design conservation plans with a special requirements at fi ner scales ( Scheidegger and Werth, 2009 ). focus on threatened species ( Balmford et al., 2005 ). Effective Therefore, it is essential to identify the environmental factors conservation strategies rely on a thorough knowledge of the life that determine the occurrence, abundance, and performance of processes and ecology of threatened species ( Hilmo and Ott, threatened species in a wide range of suitable habitats and at 2002 ; Iriondo et al., 2009 ; Scheidegger and Werth, 2009 ). The different spatial scales. viability of a population depends on two main factors: (1) popu- Few previous studies of lichens have used extensive quanti- lation size; and (2) individual performance, which are usually tative and demographic datasets over a wide geographical range associated with the habitat quality ( Soulé, 1987 ; Hilmo and Ott, to obtain critical information about the habitat requirements, 2002 ; Iriondo et al., 2009 ; Belinchón et al., 2011 ). At a large performance, and main threats for a species (but see, for ex- ample, Scheidegger and Werth, 2009 ; Hilmo et al., 2011a ; Schei et al., 2012 ). Based on this type of study, however, two 1 Manuscript received 25 February 2014; revision accepted 2 September lichen species were included as Critically Endangered in the 2014. International Union for the Conservation of Nature’s World The authors thank R. Belinchón, J.L.H. Cardós, N. Martín-Robles, P. Red List of Threatened Species ( www.iucnredlist.org ) because Matos, A.M.L. Peralta, E. Polaina, M.A.G. Otá lora, D.S. Pescador, and K. of their limited distribution and declining populations, i.e., the Walte for fi eld assistance. Special thanks to P. Matos for guiding us to the epiphyte cyanolichen Erioderma pedicellatum (Hue) P. M. Jørg Portuguese locations. We also acknowledge the staff in the protected areas and the terrestrial Cladonia perforata A. Evans ( Scheidegger, for granting permissions. This research was supported fi nancially by the Spanish Ministry of Science and Innovation (project “EPICON”, CGL2010- 2003 ; Yahr, 2003 ). For example, the accurate population analy- 22049), Comunidad Autónoma de Madrid (project “REMEDINAL2”, sis, demographic monitoring, and identifi cation of the causes of S2009/AMB-1783), and by a FPU fellowship awarded to S. Merinero by the decline of E. pedicellatum (commercial forestry and acid the Spanish Education Ministry. D.E. Jackson revised the English. We also rain) ( Cameron et al., 2013 ; Stehn et al., 2013 ) led to the imple- thank L. Concostrina-Zubiri and three anonymous reviewers for their mentation of conservation strategies to facilitate its recovery comments on the manuscript. and maintenance in Canada, including the avoidance of forestry 2 Author for correspondence (email: [email protected] ; sonia. in occupied and potential suitable habitats ( Environment [email protected]) Canada, 2007 ). Similarly, detailed knowledge of the environmen- doi:10.3732/ajb.1400077 tal requirements of the endemic species C. perforata also led to the American Journal of Botany 101 ( 11 ): 1876 – 1885 , 2014 ; http://www.amjbot.org/ © 2014 Botanical Society of America 1876 November 2014] MERINERO ET AL.— LOBARINA SCROBICULATA ECOLOGY AT MULTIPLE SCALES 1877 establishment of habitat protection measures and reintroduc- scale (Central Spain). However, there is still a lack of exhaus- tions ( Yahr, 2003 ). tive demographic data for this species, such as its population Lichens represent an important component of the terrestrial size and/or population structure, thereby suggesting that there is biodiversity, especially in forests where they are among the a need for new evidence to reassess the conservation status of dominant epiphytic organisms ( Wein and Speer, 1975 ; Aragón this species in its current geographic range. et al., 2010 ), and they have critical roles in ecosystem function- As a consequence of its rarity and ecological importance, Lo- ing, i.e., water and mineral cycles, shelter for microfauna, and barina scrobiculata has been a target species in many ecologi- food webs (reviewed by Ellis, 2012 ). Lichens are poikilohydric cal and population studies in boreal forests (e.g., Hallingbäck, organisms, i.e., they lack specialized mechanisms for regulat- 1989 ; Hilmo, 2002 ; Hilmo et al., 2011a , 2011b ; Asplund et al., ing their water content, which is controlled passively by the 2010 ; Larsson and Gauslaa, 2011 ). However, the macroenvi- water potential of the environment ( Nash, 2008 ). Thus, the dis- ronmental conditions and forest history in North America and tribution and performance of lichens are determined greatly by Northern Europe differ from those in Southern Europe, where the macro- and microclimate conditions, especially water and the ecology and habitat requirements of this species are poorly light availability, and their ranges of tolerance for these condi- characterized. Thus, the main aim of the current study was to tions, as well as other factors (i.e., suitable habitat availability, elucidate the environmental factors that modulate the occur- nutrient availability, and/or air pollution) ( Nash, 2008 ; Ellis rence, abundance, spatial distribution, and performance of L. et al., 2009 ; Ellis, 2012 ; Marini et al., 2011 ). Therefore, changes scrobiculata in the Iberian Peninsula at multiple scales. We ex- in microclimate conditions, such as those induced by forest amined representative L. scrobiculata populations throughout management, affect the diversity of epiphytic lichens, espe- the Iberian Peninsula to identify differences in the performance cially cyanolichens (i.e., lichens with cyanobacteria as the main of this species between the Atlantic and Mediterranean biogeo- photobiont) ( Gauslaa et al., 2001 ; Aragón et al., 2010 ; Ellis, graphical regions, with a specifi c focus on the latter. In the 2012 ). Cyanolichens are particularly sensitive to humidity be- Mediterranean Basin, the climatic conditions may be particu- cause they require liquid water to activate photosynthesis larly harsh for L. scrobiculata due to the physiological stress ( Lange et al., 1986 ), thus their distribution is generally con- caused by low humidity during the long summer drought trolled by the annual precipitation (see Marini et al., 2011 ). ( Valladares et al., 2004 ), and these conditions might become even Cyanolichens play signifi cant roles in the nutrient cycles in for- more extreme as a consequence of global warming ( Giménez- ests because they fi x atmospheric nitrogen ( Nash, 2008 ; Ellis, Benavides et al., 2007 ). We hypothesized that the abundance of 2012 ). Thus, given the importance of cyanolichens for ecosys- L. scrobiculata would increase with annual precipitation, which tem functioning, species-specifi c studies are required to better is consistent with the requirements of cyanolichens. Therefore,
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