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Plant Ecology

, Volume 220, Issue 11, pp 1071–1084 | Cite as

Surface roots as a new ecological zone for occurrence of vascular epiphytes: a case study on Pseudobombax trees on inselbergs

  • Dayvid Rodrigues CoutoEmail author
  • Talitha Mayumi Francisco
  • Mário Luís Garbin
  • Henrique Machado Dias
  • Miriam Cristina A. Pereira
  • Luiz Menini Neto
  • José Eduardo Macedo Pezzopane
Article
  • 67 Downloads

Abstract

This study aimed to quantify the importance of surface roots as phorophyte ecological zones for vascular epiphytes in the lithophyte tree Pseudobombax. The study was conducted on phorophytes, trees that support epiphytes, in three neotropical granitoid rocky outcrops (inselbergs). We investigated how community composition and abundance of vascular epiphytes differed among different ecological zones and examined habitat associations on Pseudobombax. Based on a census of 90 trees, we found 5896 individual vascular epiphytes attributed to 137 species. Bromeliads and orchids were dominant. Our results show that surface roots represented an important ecological zone as 53% of the diversity and 20% of the total vascular epiphyte abundance were found within this zone. Abundance patterns differed among the zones and the lithophyte species Sinningia speciosa, Selaginella convoluta and Alcantarea patriae were associated with the surface roots. Our results reinforce the importance of the lithophyte tree Pseudobombax for the maintenance of epiphytic diversity in the tropical inselbergs of southeast Brazil, mainly due to its size and architecture. The presence of large surface roots considerably increases the habitat for different epiphytic groups, including species typical of inselbergs. Roots are thus an important ecological zone for epiphytic communities on inselbergs.

Keywords

Community structure Holoepiphytes Johansson’s zones Lithophytes flora Metacommunity Neotropical 

Notes

Acknowledgements

The authors would like to express their thanks to the three anonymous reviewers and to editor Karen Harper for their valuable comments and suggestions on the manuscript; the Couto Mazza Family for granting access to their site (Pedra dos Pontões) and the ICMBio for support in the Caparaó National Park. We also thank Dr. Rodrigo de Andrade Kersten for suggestions for the methodology and the Instituto Nacional da Mata Atlântica (INMA) for granting us free access to the herbarium collection. We are grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship granted to the first author. This research was part of the master’s dissertation of the first author, in the postgraduate program of Forest Sciences of the Federal University of Espírito Santo, Brazil.

Supplementary material

11258_2019_976_MOESM1_ESM.docx (40 kb)
Supplementary file1 (DOCX 40 kb)

References

  1. Ab’sáber AN (1994/1995). No domínio das caatingas. In: Monteiro S, Kaz L (eds.). Caatinga-Sertão Sertanejos, Livroarte, Rio de Janeiro, pp. 37–46Google Scholar
  2. Alves RJV, Kolbek J, Becker J (2008) Vascular epiphyte vegetation in rocky savannas of southeastern Brazil. Nordic J Bot 26:101–117Google Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Andrades R, Machado FS, Reis-Filho JA, Macieira RM, Giarrizzo T (2018) Intertidal biogeographic subprovinces: local and regional factors shaping fish assemblages. Front Mar Sci 5:1–14Google Scholar
  5. Angelini C, Silliman BR (2014) Secondary foundation species as drivers of trophic and functional diversity: evidence from a tree–epiphyte system. Ecol 95:185–196Google Scholar
  6. APG (Angiosperm Phylogeny Group) (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linnean Soc 181:1–20Google Scholar
  7. Barthlott W, Porembski S (2000) Vascular plants on inselbergs: systematic overview. In: Porembski S, Barthlott W (eds) Inselbergs—biotic diversity of isolated rock outcrops in tropical and temperate regions. Springer, Berlin, pp 103–116Google Scholar
  8. Benzing DH (1990) Vascular epiphytes. Cambridge University Press, New YorkGoogle Scholar
  9. Boelter CR, Dambros CS, Nascimento HEM, Zartman CE (2014) A tangled web in tropical tree-tops: effects of edaphic variation, neighbourhood phorophyte composition and bark characteristics on epiphytes in a central Amazonian forest. J Veg Sci 25:1090–1099Google Scholar
  10. Burke A (2002) Island-matrix relationships in Nama Karoo inselberg landscapes. Part I: do inselbergs provide a refuge for matrix species? Plant Ecol 160:70–90Google Scholar
  11. Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples, Version 9. User’s Guide and application. https://purl.oclc.org/estimates. Accessed 23 Jan 2017
  12. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, AustriaGoogle Scholar
  13. Couto DR, Dias HM, Pereira MCA, Fraga CN, Pezzopane JEM (2016) Vascular epiphytes on Pseudobombax (Malvaceae) in rocky outcrops (inselbergs) in Brazilian Atlantic Rainforest: basis for conservation of a threatened ecosystem. Rodriguésia 67:583–601Google Scholar
  14. Crawley MJ (2013) The R Book, 2nd edn. Wiley, ChichesterGoogle Scholar
  15. Da Rocha WD, Neves FS, Dáttilo W, Delabie JHC (2016) Epiphytic bromeliads as key components for maintenance of ant diversity and ant–bromeliad interactions in agroforestry system canopies. For Ecol Manag 372:128–136Google Scholar
  16. De Paula LFA, Forzza RC, Neri AV, Bueno ML, Porembski S (2016) Sugar Loaf Land in south-eastern Brazil: a centre of diversity for mat-forming bromeliads on inselbergs. Bot J Linnean Soc 181:459–476Google Scholar
  17. Ding Y, Liu G, Zang R, Zhang J, Lu X, Jihong Huang J (2016) Distribution of vascular epiphytes along a tropical elevational gradient: disentangling abiotic and biotic determinants. Sci Rep 6:19706.  https://doi.org/10.1038/srep19706 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dislich R, Mantovani W (2016) Vascular epiphyte assemblages in a Brazilian Atlantic Forest fragment: investigating the effect of host tree features. Plant Ecol 217:1–12Google Scholar
  19. Flores-Palacios A (2016) Does structural parasitism by epiphytes exist? A case study between Tillandsia recurvata and Parkinsonia praecox. Plant Biol 18:463–470PubMedGoogle Scholar
  20. Francisco TM, Garbin ML, Castanho CT, Ruiz-Miranda CR (2018a) An overview on epiphytism as a direct mechanism of facilitation in tropical forests. Trop Ecol 59:1–9Google Scholar
  21. Francisco TM, Couto DR, Evans DM, Garbin ML, Ruiz-Miranda CR (2018b) Structure and robustness of an epiphyte–phorophyte commensalistic network in a neotropical inselberg. Austral Ecol.  https://doi.org/10.1111/aec.12640 CrossRefGoogle Scholar
  22. Freitas L, Salino A, Menini Neto L et al (2016) A comprehensive checklist of vascular epiphytes of the Atlantic Forest reveals outstanding endemic rates. PhytoKeys 58:65–79Google Scholar
  23. Furtado SG, Menini Neto L (2015) Diversity of vascular epiphytes in two high altitude biotopes of the Brazilian Atlantic Forest. Braz J Bot 38:295–310Google Scholar
  24. Gentry AH, Dodson CH (1987) Contribution of non trees to species richness of a tropical rain forest. Biotropica 19:149–156Google Scholar
  25. Gotelli NJ, Colwell RK (2011) Estimating species richness. In: Magurran AE, McGill BJ (eds) Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, pp 39–54Google Scholar
  26. Hayward RM, Martin TE, Utteridge TMA, Mustari AH, Marshall AR (2017) Are neotropical predictors of forest epiphyte–host relationships consistent in Indonesia? J Trop Ecol.  https://doi.org/10.1017/S0266467416000626 CrossRefGoogle Scholar
  27. Johansson DR (1974) Ecology of vascular epiphytes in West African rain forest. Acta Phytogeogr Suec 59(59):1–129Google Scholar
  28. Krömer T, Kessler M (2006) Filmy ferns (Hymenophyllaceae) as high-canopy epiphytes. Ecotropica 12:57–63Google Scholar
  29. Krömer T, Kessler M, Gradstein SR (2007) Vertical stratification of vascular epiphytes in submontane and montane forest of the Bolivian Andes: the importance of the understory. Plant Ecol 189:261–278Google Scholar
  30. Li S, Liu WY, Li DA-W et al (2015) Species richness and vertical stratification of epiphytic lichens in subtropical primary and secondary forests in southwest China. Fungal Ecol 17:30–40Google Scholar
  31. Magalhães JLL, Lopes MA (2015) Species richness and abundance of low-trunk herb epiphytes in relation to host tree size and bark type, eastern Amazonia. Rev Árvore 39:457–466Google Scholar
  32. Marí MLG, Toledo JJ, Nascimento HEM, Zartman CE (2016) Regional and fine scale variation of holoepiphyte community structure in central amazonian white-sand forests. Biotropica 48:70–80Google Scholar
  33. McArdle BBH, Anderson M (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297Google Scholar
  34. Menini Neto L, Forzza RC, Zappi D (2009) Angiosperm epiphytes as conservation indicators in forest fragments: A case study from southeastern Minas Gerais, Brazil. Biodivers Conserv 18:3785–3807Google Scholar
  35. Menini Neto L, Van Den Berg C, Forzza RC (2013) Taxonomic revision of Pseudolaelia Porto & Brade (Laeliinae, Orchidaceae). Acta Bot Brasil 27:418–435Google Scholar
  36. Nieder J, Prosperi J, Michaloud G (2001) Epiphytes and their contribution to canopy diversity. Plant Ecol 153:51–63Google Scholar
  37. Obermüller FA, Silveira M, Salimon CI, Daly DC (2012) Epiphytic (including hemiepiphytes) diversity in three timber species in the southwestern Amazon, Brazil. Biodivers Conserv 21:565–575Google Scholar
  38. Oksanen F, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) Vegan: community ecology package. R package version 2.5-2. https://CRAN.R-project.org/package-vegan
  39. Perry DR (1978) A method of access into the crowns of emergent and canopy trees. Biotropica 10:155–157Google Scholar
  40. Porembski S (2003) Epiphytic orchids on arborescent Velloziaceae and Cyperaceae: Extremes of phorophyte specialisation. Nordic J Bot 23:505–512Google Scholar
  41. Porembski S (2007) Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Braz Jot 30:579–586Google Scholar
  42. Porembski S, Barthlott W (2000) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecol 151:19–28Google Scholar
  43. PPG (Pteridophyte Phylogeny Group) (2016) A community-derived classification for extant lycophytes and ferns. PPG I J Syst Evol 54:563–603Google Scholar
  44. Sanford WW (1968) Distribution of epiphytic orchids in semi-deciduous tropical forest in southern Nigeria. J Ecol 56:697–705Google Scholar
  45. Sanger JC, Kirkpatrick JB (2015) Moss and vascular epiphyte distri- butions over host tree and elevation gradients in Australian subtropical rainforest. Austral J Bot 63:696–704Google Scholar
  46. Sanger JC, Kirkpatrick JB (2016) Fine partitioning of epiphyte habitat within Johansson zones in tropical Australian rain forest trees. Biotropica 47:27–34Google Scholar
  47. Sporn SG, Bos MM, Kessler M, Gradstein SR (2010) Vertical distribution of epiphytic bryophytes in an Indonesian rainforest. Biodivers Conserv 19:745–760Google Scholar
  48. Taylor A, Burns K (2015) Epiphyte community development throughout tree ontogeny: an island ontogeny framework. J Veg Sci 46:902–910Google Scholar
  49. Thiers B [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/ih/. Accessed 05 Jan 2019Google Scholar
  50. Wang X, Long W, Schamp BS et al (2016) Vascular epiphyte diversity differs with host crown zone and diameter, but not orientation in a Tropical Cloud Forest. PLoS ONE 11:e0158548PubMedPubMedCentralGoogle Scholar
  51. Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101Google Scholar
  52. Werneck MS, Espirito-Santo MM (2002) Species diversity and abundance of vascular epiphytes on Vellozia piresiana in Brasil. Biotropica 34:51–57Google Scholar
  53. Woods CL, Cardelús CL, Dewalt SJ (2015) Microhabitat associations of vascular epiphytes in a wet tropical forest canopy. J Ecol 103:421–430Google Scholar
  54. Xu HQ, Liu WY (2005) Species diversity and distribution of epiphytes in the montane moist evergreen broad–leaved forest in Ailao Mountain, Yunnan. Biodivers Sci 13:137–147Google Scholar
  55. Zhao M, Geekiyanage N, Xu J et al (2015) Structure of the epiphyte community in a tropical montane forest in SW China. PLoS ONE 10:e0122210PubMedPubMedCentralGoogle Scholar
  56. Zotz G (2007) Johansson revisited: the spatial structure of epiphyte assemblages. J Veg Sci 18:123–130Google Scholar
  57. Zotz G (2013) The systematic distribution of vascular epiphytes-a critical update. Bot J Linn Soc 171:453–481Google Scholar
  58. Zotz G (2016) Plants on plants—the biology of vascular epiphytes. Springer, New YorkGoogle Scholar
  59. Zotz G, Budel B, Meyer A, Zellner H, Lange OL (1997) Water relations and CO2 exchange of tropical bryophytes in a lower montane rainforest in Panama. Acta Bot 110:9–17Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Programa de Pós-Graduação Em Ciências FlorestaisUniversidade Federal do Espírito Santo, Centro de Ciências Agrárias e EngenhariasJerônimo MonteiroBrazil
  2. 2.Programa de Pós-Graduação Em Ecologia E Recursos Naturais, Laboratório de Ciências AmbientaisUniversidade Estadual Do Norte Fluminense Darcy RibeiroCampos dos GoytacazesBrazil
  3. 3.Departamento de BiologiaUniversidade Federal do Espírito Santo, Centro de Ciências Exatas, Naturais e da SaúdeAlegreBrazil
  4. 4.Programa de Pós-graduação Em Ciências FlorestaisUniversidade Federal do Espírito Santo, Centro de Ciências Agrárias e EngenhariasJerônimo MonteiroBrazil
  5. 5.Programa de Pós-Graduação Em EcologiaInstituto de Ciências Biológicas, Universidade Federal de Juiz de ForaJuiz de ForaBrazil

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