Ecological Research

, Volume 32, Issue 4, pp 503–509 | Cite as

Tree hollows can affect epiphyte species composition

  • Shinichi Tatsumi
  • Takayuki Ohgue
  • Wakana Azuma
  • Veera Tuovinen
  • Yume Imada
  • Akira S. Mori
  • Göran Thor
  • Åsa Ranlund
Original Article


Tree hollows often harbor animals and microorganisms, thereby storing nutritive resources derived from their biological activities. The outflows from tree hollows can create unique microenvironments, which may affect communities of epiphytic organisms on trunk surfaces below the hollows. In this study, we tested whether the species richness and composition of epiphytic bryophytes (liverworts and mosses) and lichens differ above and below tree hollows of Aria japonica and Cercidiphyllum japonicum in a Japanese temperate forest. The species richness of epiphytic bryophytes and lichens did not differ above and below hollows; however, the species composition of bryophytes differed significantly above and below hollows. Indicator species analyses showed that the moss species Anomodon tristis and the liverwort species Porella vernicosa were significantly more common below than above hollows, while the liverwort species Radula japonica and four lichen species, including Leptogium cyanescens, occurred more frequently above than below hollows. Our results highlight that tree hollows can produce unique microenvironments on trunk surfaces that potentially contribute to the maintenance of epiphytic diversity on a local scale.


Biodiversity Cryptogams Bryophytes Lichens Tree cavities 



This study was partly conducted as part of the postgraduate course Ecological Research in Practice: A Field Based Course in Japan organized by the Swedish University of Agricultural Sciences. We thank Tatsuhiro Ohkubo for kindly arranging the collection permits, and Lena Gustafsson and Matthew Low for their assistance during the course. We are also grateful to Ryo Kitagawa, Keiichi Okada, two anonymous reviewers, and the Associate Editor-in-Chief (Yusuke Onoda) for insightful comments on earlier versions of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11284_2017_1468_MOESM1_ESM.pdf (45 kb)
Supplementary material 1 (PDF 45 kb)


  1. Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ, Cornell HV, Comita LS, Davies KF, Harrison SP, Kraft NJB, Stegen JC, Swenson NG (2011) Navigating the multiple meanings of beta diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28CrossRefPubMedGoogle Scholar
  2. Anderson DL, Koomjian W, French B, Altenhoff SR, Luce J (2015) Review of rope-based access methods for the forest canopy: safe and unsafe practices in published information sources and a summary of current methods. Methods Ecol Evol 6:865–872CrossRefGoogle Scholar
  3. Barkman JJ (1958) Phytosociology and ecology of cryptogamic epiphytes: including a taxonomic survey and description of their vegetation units in Europe. Van Gorcum, Assen, p 628Google Scholar
  4. Bates D, Maechler M, Bolker BM, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  5. Brunet J, Fritz Ö, Richnau G (2010) Biodiversity in European beech forests—a review with recommendations for sustainable forest management. Ecol Bull 53:77–94Google Scholar
  6. Cáceres MD, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574CrossRefPubMedGoogle Scholar
  7. Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:art24CrossRefGoogle Scholar
  8. Coffey D, Andersen T (2012) Best practices for SRT in arboriculture. Tree Care Industry Association, New Hampshire, p 120Google Scholar
  9. Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  10. de Oliveira SM, ter Steege H (2015) Bryophyte communities in the Amazon forest are regulated by height on the host tree and site elevation. J Ecol 103:441–450CrossRefGoogle Scholar
  11. Derraik JGB, Heath ACG (2010) Immature Diptera (excluding Culicidae) inhabiting phytotelmata in the Auckland and Wellington regions. New Zeal J Mar Freshw Res 39:981–987CrossRefGoogle Scholar
  12. Dickinson TA, Tanner EVJ (1978) Exploitation of hollow trunks by tropical trees. Biotropica 10:231–233CrossRefGoogle Scholar
  13. Ellis CJ (2012) Lichen epiphyte diversity: a species, community and trait-based review. Perspect Plant Ecol Evol Syst 14:131–152CrossRefGoogle Scholar
  14. Ellis CJ, Eaton S, Theodoropoulos M, Elliott K (2015) Epiphyte communities and indicator species: an ecological guide for Scotland’s woodlands. Royal Botanic Garden Edinburgh, Edinburgh, p 136Google Scholar
  15. Fritz Ö, Heilmann-Clausen J (2010) Rot holes create key microhabitats for epiphytic lichens and bryophytes on beech (Fagus sylvatica). Biol Cons 143:1008–1016CrossRefGoogle Scholar
  16. Gow EA, Wiebe KL, Musgrove A (2015) Nest sanitation in response to short- and long-term changes of brood size: males clean more in a sex-role-reversed species. Anim Behav 104:137–143CrossRefGoogle Scholar
  17. Iwatsuki Z (2001) Mosses and Liverworts of Japan. Tokyo, Heibonsha, p 355Google Scholar
  18. Janzen DH (1976) Why tropical trees have rotten cores. Biotropica 8:110CrossRefGoogle Scholar
  19. Johansson P, Rydin H, Thor G (2007) Tree age relationships with epiphytic lichen diversity and lichen life history traits on ash in southern Sweden. Ecoscience 14:81–91CrossRefGoogle Scholar
  20. Komposch H, Hafellner J (2000) Diversity and vertical distribution of lichens in a Venezuelan tropical lowland rain forest. Selbyana 21:11–24Google Scholar
  21. Kurokawa S, Kashiwadani H (2006) Checklist of Japanese lichens and allied fungi. Natural Science Museum, Tokyo, p 157Google Scholar
  22. Lamit LJ, Busby PE, Lau MK, Compson ZG, Wojtowicz T, Keith AR, Zinkgraf MS, Schweitzer JA, Shuster SM, Gehring CA, Whitham TG (2015) Tree genotype mediates covariance among communities from microbes to lichens and arthropods. J Ecol 103:840–850CrossRefGoogle Scholar
  23. Lange OL, Büdel B, Meyer A, Kilian E (1993) Further evidence that activation of net photosynthesis by dry cyanobacterial lichens requires liquid water. Lichenologist 25:175–189CrossRefGoogle Scholar
  24. Mežaka A, Brūmelis G, Piterāns A (2012) Tree and stand-scale factors affecting richness and composition of epiphytic bryophytes and lichens in deciduous woodland key habitats. Biodiv Cons 21:3221–3241CrossRefGoogle Scholar
  25. Nadkarni NM, Matelson TJ (1991) Fine litter dynamics within the tree canopy of a tropical cloud forest. Ecology 72:2071–2082CrossRefGoogle Scholar
  26. Nakajima A (1968) Tsukuba-san no chii mokuroku. Flora Ibaraki 40:5–6Google Scholar
  27. Oishi Y (2009) A survey method for evaluating drought-sensitive bryophytes in fragmented forests: a bryophyte life-form based approach. Biol Cons 142:2854–2861CrossRefGoogle Scholar
  28. Oksanen J, Blanchet FG, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) vegan: community ecology package. R package version 2.3-5. Accessed 1 Nov 2015
  29. Olarinmoye SO (1975) Culture studies on Radula flaccida Lindenb. & Gottsche. J Bryol 8:357–363CrossRefGoogle Scholar
  30. Ouin A, Cabanettes A, Andrieu E, Deconchat M, Roume A, Vigan M, Larrieu L (2015) Comparison of tree microhabitat abundance and diversity in the edges and interior of small temperate woodlands. For Ecol Manage 340:31–39CrossRefGoogle Scholar
  31. Perry DR (1978) Factors influencing arboreal epiphytic phytosociology in Central America. Biotropica 10:235–237CrossRefGoogle Scholar
  32. Ranius T, Johansson P, Berg N, Niklasson M (2008) The influence of tree age and microhabitat quality on the occurrence of crustose lichens associated with old oaks. J Veg Sci 19:653–662CrossRefGoogle Scholar
  33. Seaward MRD (2008) Environmental role of lichens. In: Nash TH (ed) Lichen biology. Cambridge University Press, Cambridge, pp 274–298CrossRefGoogle Scholar
  34. Sillett TS (1994) Foraging ecology of epiphyte-searching insectivorous birds in Costa Rica. Condor 96:863–877CrossRefGoogle Scholar
  35. Sporn SG, Bos MM, Kessler M, Gradstein SR (2010) Vertical distribution of epiphytic bryophytes in an Indonesian rainforest. Biodiv Cons 19:745–760CrossRefGoogle Scholar
  36. Tadakara R, Aizawa M, Ohkubo T (2014) Forest types and evidence of past forest fires in Utsunomiya University Forest in Nikko. Bull Utsunomiya Univ For 50:85–90Google Scholar
  37. Ter Steege H, Cornelissen JHC (1988) Collecting and studying bryophytes in the canopy of standing rain forest trees. In: Glime JM (ed) Methods in bryology. Hattori Bot Lab, Nichinan, pp 285–290Google Scholar
  38. Thor G, Johansson P, Jönsson MT (2010) Lichen diversity and red-listed lichen species relationships with tree species and diameter in wooded meadows. Biodivers Conserv 19:2307–2328CrossRefGoogle Scholar
  39. Van Stan JT, Pypker TG (2015) A review and evaluation of forest canopy epiphyte roles in the partitioning and chemical alteration of precipitation. Sci Total Environ 536:813–824CrossRefPubMedGoogle Scholar
  40. Voigt CC, Borissov I, Kelm DH (2015) Bats fertilize roost trees. Biotropica 47:403–406CrossRefGoogle Scholar
  41. Wilson B (1933) A bryological study of some epiphyte mosses of a Central Indiana Woods. Butler Univ Bot Studies 3:149–171Google Scholar
  42. Woods CL, Cardelús CL, DeWalt SJ (2015) Microhabitat associations of vascular epiphytes in a wet tropical forest canopy. J Ecol 103:421–430CrossRefGoogle Scholar
  43. Zhao M, Nalaka G, Xu J, Khin MM, Dian RN, Paudel E, Harrison R (2015) Structure of the epiphyte community in a tropical montane forest in SW China. PLoS One 10:e0122210CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  • Shinichi Tatsumi
    • 1
    • 5
  • Takayuki Ohgue
    • 2
  • Wakana Azuma
    • 3
    • 6
  • Veera Tuovinen
    • 4
  • Yume Imada
    • 2
  • Akira S. Mori
    • 1
  • Göran Thor
    • 4
  • Åsa Ranlund
    • 4
  1. 1.Department of Environment and Information SciencesYokohama National UniversityKanagawaJapan
  2. 2.Graduate School of Human and Environmental StudiesKyoto UniversityKyotoJapan
  3. 3.Field Science Education and Research CenterKyoto UniversityKyotoJapan
  4. 4.Department of EcologySwedish University of Agricultural SciencesUppsalaSweden
  5. 5.Department of Biological SciencesUniversity of Toronto ScarboroughTorontoCanada
  6. 6.Graduate School of AgricultureKyoto UniversityKyotoJapan

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