Supplementary Files
Keywords
community composition
corticulous lichens
Costa Rica
hemeroby
lichen diversity
Bosque nuboso
composición de la comunidad
Costa Rica
líquenes cortícolas
hemerobia
diversidad de líquenes
How to Cite
Abstract
Introduction: Lichen diversity, community structure, composition and species abundance have been used as indicators of the integrity and ecological continuity of tropical forest ecosystems. Objectives: To assess corticolous lichen species composition, diversity, and ecological importance of three forested stands differing in time of abandonment as indicators of how passive restoration influences the lichen community assemblage. Methods: We surveyed individual lichens on tree stems of a reference old secondary forest and a young secondary forest (50 and 14-year-old natural regeneration after pasture abandonment, respectively), and in a 35-year-old exotic cypress tree plantation, in the oriental Central Valley, in Orosí, Costa Rica. Standard diversity, similarity indexes, and the importance value index were calculated. An NMDS analysis was performed on the community structure parameters and in a presence-absence matrix. Results: We found 64 lichen species in 25 families with 42, 21, and 23 species, and 20, 10, and 15 families, in the young and old secondary forests, and the cypress plantation, respectively. Cryptothecia sp. possessed the highest importance across sites. More than 87 % of the species are rare. The combined IVI of the top three families were: 36, 48.5, and 74.8 % in the young and old forests and the Cypress plantation sites, respectively. Overall, Arthoniaceae is in the top three families. The young forest had the highest species richness, but the old forest presented the best evenness. Similarity and diversity indexes suggest a particularly low resemblance in the lichen communities but a smooth gradient differentiation between the three forests, which was confirmed by the NMDS test. The homogeneity test identified great differences in ecological importance and composition. Conclusions: This region contains a distinctive assemblage of species resulting in a strong community differentiation by site, reflecting the influence of ecophysiological and microclimatic factors that define lichen establishment and survival and suggesting a great regional beta diversity, within a fragmented landscape. Greater connectivity and passive restoration strategies resulted in greater diversity and a more heterogeneous community structure on both forests than the corticolous community of the abandoned plantation. Protection of forest fragments will maximize the integrity of future forests.
References
Berryman, S., & McCune, B. (2006). Estimating epiphytic macrolichen biomass from topography, stand structure and lichen community data. Journal of Vegetation Science, 17(2), 157–170. https://doi.org/10.1111/j.1654-1103.2006.tb02435.x
Bustamante, E.N., Monge-Nájera, J., & González Lutz, M.I. (2011). Air pollution in a tropical city: the relationship between wind direction and lichen bio-indicators in San José, Costa Rica. Revista de Biología Tropical, 59(2), 899–905. http://www.ncbi.nlm.nih.gov/pubmed/21717859
Cáceres, M.E.S., Lücking, R., & Rambold, G. (2007). Phorophyte specificity and environmental parameters versus stochasticity as determinants for species composition of corticolous crustose lichen communities in the Atlantic rain forest of Northeastern Brazil. Mycological Progress, 6(3), 117–136. https://doi.org/10.1007/s11557-007-0532-2
Cascante-Marín, A., Von Meijenfeldt, N., De Leeuw, H.M.H., Wolf, J.H.D., Gerard, J., Oostermeijer, B., & Den Nijs, J.C.M. (2009). Dispersal limitation in epiphytic bromeliad communities in a Costa Rican fragmented montane landscape. Journal of Tropical Ecology, 25(1), 63–73. https://doi.org/10.1017/S0266467408005622
Condit, R., Ashton, P., Balslev, H., Brokaw, N., Bunyavejchewin, S., Chuyong, G., & Zimmerman, J.K. (2005). Tropical tree a-diversity: Results from a worldwide network of large plots. Biologiske Skrifter, 55, 565–582.
Condit, R., Hubbell, S.P., Lafrankie, J.V., Sukumar, R., Manokaran, N., Foster, R.B., & Ashton, P.S. (1996). Species-area and species-individual of three 50-ha plots trees : a comparison of three 50-ha plots. Journal of Ecology, 84(4), 549–562.
Cornelissen, J.H.C., Callaghan, T.V., Alatalo, J.M., Michelsen, A., Graglia, E., Hartley, A.E., Hik, D.S., Hobbie, S.E., Press, M.C., Robinson, C.H., Henry, G.H.R., Shaver, G.R., Phoenix, G.K., Gwynn Jones, D., Jonasson, S., Chapin III, F.S., Molau, U., Neill, C., Lee, J.A., … Aerts, R. (2001). Global change and arctic ecosystems: Is lichen decline a function of increases in vascular plant biomass? Journal of Ecology, 89(6), 984–994. https://doi.org/10.1046/j.1365-2745.2001.00625.x
Cristofolini, F., Giordani, P., Gottardini, E., & Modenesi, P. (2008). The response of epiphytic lichens to air pollution and subsets of ecological predictors: a case study from the Italian Prealps. Environmental Pollution, 151(2), 308–317. https://doi.org/10.1016/j.envpol.2007.06.040
Crites, S., & Dale, M.R.T. (1998). Diversity and abundance of bryophytes, lichens, and fungi in relation to woody substrate and successional stage in aspen mixedwood boreal forests. Canadian Journal of Botany, 76(4), 641–651. https://doi.org/10.1139/b98-030
Enquist, B.J., Feng, X., Boyle, B., Maitner, B., Newman, E.A., Jørgensen, P.M., Roehrdanz, P.R., Thiers, B.M., Burger, J.R., Corlett, R.T., Couvreur, T.L.P., Dauby, G., Donoghue, J.C., Foden, W., Lovett, J.C., Marquet, P.A., Merow, C., Midgley, G., Morueta-Holme, N., … McGill, B.J. (2019). The commonness of rarity: Global and future distribution of rarity across land plants. Science Advances, 5(11), eaaz0414. https://doi.org/10.1126/sciadv.aaz0414
Estrabou, C., Stiefkens, L., Hadid, M., Rodríguez, J.M., & Pérez, A. (2005). Estudio Comparativo de la Comunidad Liquénica en Cuatro Ecosistemas de la Provincia de Córdoba. Boletín de la Sociedad Argentina de Botanica, 40(1–2), 1–10.
Fagan, W.F., & Kareiva, P.M. (1997). Using compiled species lists to make biodiversity comparisons among regions: A test case using Oregon butterflies. Biological Conservation, 80(3), 249–259. https://doi.org/10.1016/S0006-3207(96)00144-9
Galloway, D.J. (1992). Biodiversity: a lichenological perspective. Biodiversity and Conservation, 1(4), 312–323.
Gasparyan, A., Sipman, H.J.M., Marini, L., & Nascimbene, J. (2018). The inclusion of overlooked lichen microhabitats in standardized forest biodiversity monitoring. Lichenologist, 50(2), 231–237. https://doi.org/10.1017/S0024282918000087
Giordani, P. (2007). Is the diversity of epiphytic lichens a reliable indicator of air pollution? A case study from Italy. Environmental Pollution, 146(2), 317–323. https://doi.org/10.1016/j.envpol.2006.03.030
Heltshe, J.F., & Forrester, N.E. (1983). Estimating species richness using the jackknife procedure. Biometrics, 39, 1–11.
Honegger, R. (1991). Functional aspects of the lichen symbiosis. Annual Review of Plant Biology, 42, 553–578.
Hubbell, S.P. (2001). The unified neutral theory of biodiversity and biogeography. Princeton University Press.
Krebs, C.J. (1999). Ecological methodology. Addison.
Legendre, P., & Gallagher, E.D. (2001). Ecologically meaningful transformations for ordination of species data. Oecologia, 129(2), 271–280.
Lehmkuhl, J.F. (2004). Epiphytic lichen diversity and biomass in low-elevation forests of the eastern Washington Cascade Range, USA. Forest Ecology and Management, 187(2–3), 381–392. https://doi.org/10.1016/j.foreco.2003.07.003
López, W., & Duque, Á. (2010). Patrones de diversidad alfa en tres fragmentos de bosques montanos en la región norte de los Andes, Colombia. Revista de Biología Tropical, 58(1), 483–498.
Lücking, R. (1999a). Ecology of Folicolous Lichens at the "Botarrama" Trail (Costa Rica), a Neotropical Rain Forest . I. Species Composition and its Ecogeographical Implications 1. Biotropica, 31(4), 553–564.
Lücking, R. (1999b). Líquenes folícolas de la Estación Biológica La Selva, Costa Rica: Inventario, comunidades y comparación florística de tipos de vegetación. Revista Biología Tropical, 47(3), 287–308.
Lücking, R., Moncada, B., Martínez-Habibe, M.C., Salgado-Negret, B.E., Celis, M., Rojas-Zamora, O., Rodrígez-M, G.M., Brokamp, G., & Borsch, T. (2019). Lichen diversity in Colombian Caribbean dry forest remnants. Caldasia, 41(1), 194-214.
McCune, B. (2000). New Frontiers in Bryology and Lichenology Lichen Communities as Indicators of Forest Health. The Bryologist, 103(2), 353–356.
Monge-Nájera, J., González, M.I., Rivas, M., & Méndez-Estrada, V.H. (2002). A new method to assess air pollution using lichens as bioindicators. Revista Biología Tropical, 50(1), 321–325. http://www.ncbi.nlm.nih.gov/pubmed/12298260
Neitlich, P., & McCune, B. (1997). Hotspots of lichen diversity in Two young managed forests. Conservation Biology, 11(1), 172–182.
Neurohr, E., Monge-Nájera, J., & González-Lutz, M. (2011). Air pollution in a tropical city: the relationship between wind direction and lichen bio-indicators in San José, Costa Rica. Revista Biología Tropical, 59(2), 889–905.
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Henry, M., Stevens, H., & Wagner, H. (2014). Vegan Community Ecology Package. (Version 2.2-0., R Package). https://www.scirp.org/(S(351jmbntvnsjt1aadkposzje))/reference/ReferencesPapers.aspx?ReferenceID=1778707
Ortiz-Malavassi, E. (2014). Atlas digital de Costa Rica 2014. Tecnológico de Costa Rica. https://hdl.handle.net/2238/6749
Palmer, M.W. (1990). The Estimation of Species Richness by Extrapolation. Ecology, 71(3), 1195–1198. https://doi.org/10.2307/1937387
Petrokas, R., & Baliuckas, V. (2017). Self-sustaining forest. Applied Ecology and Environmental Research, 15(4), 409–426.
Pinokiyo, A., Singh, K.P., & Singh, J.S. (2008). Diversity and distribution of lichens in relation to altitude within a protected biodiversity hot spot, north-east India. Lichenologist, 40(1), 47–62.
Polo, C. (2008). Índices más comunes en biología. Segunda parte, similaridad y riqueza beta y gamma. Revista Facultad de Ciencias Básicas, 4(1–2), 135–142.
Proctor, M.C. (2014). The diversification of bryophytes and vascular plants in evolving terrestrial environments. In D.T. Janson & S.K. Rice (Eds.), Photosynthesis in bryophytes and early land plants (pp. 59–77). Springer.
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org/
Rivas-Plata, E., Lücking, R., & Lumbsch, H.T. (2008). When family matters: An analysis of Thelotremataceae (Lichenized Ascomycota: Ostropales) as bioindicators of ecological continuity in tropical forests. Biodiversity and Conservation, 17(6), 1319–1351. https://doi.org/10.1007/s10531-007-9289-9
Santos, V.M., Cáceres, M.E.S., & Lücking, R. (2020). Diversity of foliicolous lichens in isolated montane rainforests (Brejos) of northeastern Brazil and their biogeography in a neotropical context. Ecological Research, 35(1), 182–197. https://doi.org/10.1111/1440-1703.12071
Sipman, H.J. (2020). Identification key and literature guide to the genera of Lichenized Fungi (Lichens) in the Neotropics. Botanic Garden & Botanical Museum Berlin-Dahlem. https://archive.bgbm.org/BGBM/STAFF/Wiss/Sipman/keys/neokeyA.htm
Sipman, H.J., Lücking, R., Aptroot, A., Chaves, J.L., Kalb, K., & Tenorio, L.U. (2012). A first assessment of the Ticolichen biodiversity inventory in Costa Rica and adjacent areas: the thelotremoid Graphidaceae (Ascomycota: Ostropales). Phytotaxa, 55(1), 1–214. https://doi.org/10.11646/phytotaxa.55.1.1
Spake, R., Ezard, T.H.G., Martin, P.A., Newton, A.C., & Doncaster, C.P. (2015). A meta-analysis of functional group responses to forest recovery outside of the tropics. Conservation Biology, 29(6), 1695–1703. https://doi.org/10.1111/cobi.12548
Thüs, H., Wolseley, P., Carpenter, D., Eggleton, P., Reynolds, G., Vairappan, C.S., Weerakoon, G., & Mrowicki, R.J. (2021). Key Roles of Dipterocarpaceae, Bark Type Diversity and Tree Size in Lowland Rainforests of Northeast Borneo–Using Functional Traits of Lichens to Distinguish Plots of Old Growth and Regenerating Logged Forests. Microorganisms, 9(3), 541. https://doi.org/10.3390/microorganisms9030541
Will-Wolf, S., Geiser, L.H., Neitlich, P., & Reis, A.H. (2006). Forest lichen communities and environment–How consistent are relationships across scales? Journal of Vegetation Science, 17(2), 171. https://doi.org/10.1658/1100-9233(2006)17[171:flcaec]2.0.co;2
Williams, L., & Ellis, C.J. (2018). Ecological constraints to ‘old-growth’lichen indicators: niche specialism or dispersal limitation? Fungal Ecology, 34, 20–27
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2021 Roberto A. Cordero S., Ana Garrido, Junior Pastor Pérez-Molina, Óscar Ramírez-Alán, José Luis Chávez