Diversity of wood-inhabiting fungi in woodpecker nest cavities in southern Poland

Robert Jankowiak, Michał Ciach, Piotr Bilański, Riikka Linnakoski

Abstract


Globally, tree-holes are important ecological component of forest and woodlands. Numerous microorganisms rely on cavities, both natural and those excavated by primary cavity nesting birds, mainly by woodpeckers, for their survival and reproduction. However, the fungi occurring in cavities are not well characterized. Specifically, very little is known about the fungal communities inhabiting the woodpecker nest cavities. Therefore, in this study, we investigated the fungal diversity of cavities in southern Poland. The samples were collected from freshly excavated woodpecker nest cavities using a nondestructive method (ND). The spatial distribution of fungal communities within the cavities was evaluated by sampling different parts of a single cavity using a destructive method (D). We detected 598 fungal isolates that included 64 species in three phyla and 16 orders using the ND method. Most of the fungi isolated from the cavities represented the phylum Ascomycota (73.9% of the isolates) with 11 orders, and Microascales was the predominant order (30% of the isolates). The most common species detected was Petriella musispora, which was isolated from 65% of the cavities. A total of 150 isolates (25%) were members of Basidiomycota, with Hymenochaetales being the dominant order (16% of the isolates). The basidiomycetous fungi were isolated from 55% of the cavities. Several taxa closely related to the pathogenic fungi and associated with secondary animal infections were detected in the wood of cavities. We identified different fungal communities in the three cavity parts using the D method. The cavity entrance had more number of species than the middle and bottom parts. The results of this study advanced our current knowledge on the mycobiota in woodpecker nest cavities and provided preliminary evidence for tree cavities being the hotspot for fungal diversity.

Keywords


Basidiomycetes; cavity; Microascales; wood-inhabiting fungi; wood-decay fungi; woodpeckers; tree-hollow

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References


Wesołowski T, Martin K. Tree holes and hole-nesting birds in European and North American forests. In: Mikusiński G, Roberge JM, Fuller RT, editors. The ecology and conservation of forest birds. Cambridge: Cambridge University Press; 2018. p. 79–133. https://doi.org/10.1017/9781139680363.006

Lieutier F, Day KR, Battisti A, Gregoire JC, Evans HF. Bark and wood boring insects in living trees in Europe: a synthesis. Dordrecht: Kluwer Academic Publishers; 2004. https://doi.org/10.1007/1-4020-2241-7

Cockle KL, Martin K, Robledo G. Linking fungi, trees, and hole-using birds in a Neotropical tree-cavity network: pathways of cavity production and implications for conservation. For Ecol Manage. 2012;264:210–219. https://doi.org/10.1016/j.foreco.2011.10.015

Martin K, Aitken KEH, Wiebe KL. Nest sites and nest webs for cavity-nesting communities in interior British Columbia, Canada: nest characteristics and niche partitioning. Condor. 2004;106:5–19. https://doi.org/10.1650/7482

Hart JH, Hart DL. Heartrot fungi’s role in creating Picid nesting sites in living aspen. In: Symposium proceedings: “Sustaining aspen in western landscape”; 2000 Jun 13–15; Grand Junction, CO, USA. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station; 2001. p. 207–213. (Proceedings RMRS; vol 18).

Jackson AJ, Jackson BJ. Ecological relationships between fungi and woodpecker cavity sites. Condor. 2004;106:37–49. https://doi.org/10.1650/7483

Zahner V, Sikora L, Pasinelli G. Heart rot as a key factor for cavity tree selection in the black woodpecker. For Ecol Manage. 2012;271:98–103. https://doi.org/10.1016/j.foreco.2012.01.041

Jusino MA, Lindner DL, Banik MT, Walters JR. Heart rot hotel: fungal communities in red cockaded woodpecker excavations. Fungal Ecol. 2015;14:33–43. https://doi.org/10.1016/j.funeco.2014.11.002

Pasinelli G. Population biology of European woodpecker species: a review. Ann Zool Fennici. 2006;43:96–111.

Blanc LA, Martin K. Identifying suitable woodpecker nest trees using decay selection profiles in trembling aspen (Populus tremuloides). For Ecol Manage. 2012;286:192–202. https://doi.org/10.1016/j.foreco.2012.08.021

Lõhmus A. Habitat indicators for cavity-nesters: the polypore Phellinus pini in pine forests. Ecol Indic. 2016;66:275–280. https://doi.org/10.1016/j.ecolind.2016.02.003

Conner RN, Locke BA. Fungi and red-cockaded woodpecker cavity trees. Wilson Bull. 1982;94:64–70.

Jusino MA, Lindner DL, Banik MT, Rose KR, Walters JR. Experimental evidence of a symbiosis between red-cockaded woodpeckers and fungi. Proc R Soc B. 2016;283:20160106. https://doi.org/10.1098/rspb.2016.0106

Glutz von Blotzheim UN, Bauer K. Handbuch der Vögel Mitteleuropas. Vol. 9. Columbiformes-Piciformes. Wiesbaden: Aula-Verlag; 1980.

Gorman G. The black woodpecker – a monograph on Dryocopus martius. Barcelona: Lynx Edicions; 2011.

Sedgeley JA. Quality of cavity microclimate as a factor influencing selection of maternity roosts by a tree-dwelling bat, Chalinolobus tuberculatus, in New Zealand. J Appl Ecol. 2001;38:425–438. https://doi.org/10.1046/j.1365-2664.2001.00607.x

Wiebe KL. Microclimate of tree cavity nests: is it important for reproductive success in northern flickers? Auk. 2001;118:412–421. https://doi.org/10.2307/4089802

Grüebler MU, Widmer S, Korner-Nievergelt F, Naef-Daenzer B. Temperature characteristics of winter roost-sites for birds and mammals: tree cavities and anthropogenic alternatives. Int J Biometeorol. 2014;58:629–637. https://doi.org/10.1007/s00484-013-0643-1

Maziarz M, Wesołowski T. Microclimate of tree cavities used by great tits (Parus major) in a primeval forest. Avian Biol Res. 2013;6:47–56. https://doi.org/10.3184/175815513X13611994806259

Maziarz M, Broughton RK, Wesołowski T. Microclimate in tree cavities and nest-boxes: implications for hole-nesting birds. For Ecol Manage. 2017;389:306–313. https://doi.org/10.1016/j.foreco.2017.01.001

Gotzman J, Jabłoński B. Gniazda naszych ptaków. Warszawa: PZWS; 1972.

Kozma JM, Kroll AJ. Nestling provisioning by hairy and white-headed woodpeckers in managed ponderosa pine forests. Wilson J Ornithol. 2013;125:534–543. https://doi.org/10.1676/12-188.1

Bodrati A, Cockle KL, Di Sallo FG, Ferreyra C, Salvador SA, Lammertink M. Nesting and social roosting of the ochre-collared piculet (Picumnus temminckii) and white-barred piculet (Picumnus cirratus), and implications for the evolution of woodpecker (picidae) breeding biology. Ornitol Neotrop. 2015;26:223–244.

Heenan CB. An overview of the factors influencing the morphology and thermal properties of avian nests. Avian Biol Res. 2013;6:104–118. https://doi.org/10.3184/003685013X13614670646299

Apinis AE, Pugh GJF. Thermophilous fungi of birds’ nests. Mycopathol Mycol Appl. 1967;33:1–9. https://doi.org/10.1007/BF02049784

Kowalski T. Oak decline: I. Fungi associated with various disease symptoms on overground portions of middle-aged and old oak (Quercus robur L.). Eur J Forest Pathol. 1991;21:136–151. https://doi.org/10.1111/j.1439-0329.1991.tb01418.x

Kamgan Nkuekam G, Solheim H, de Beer ZW, Grobbelaar C, Jacobs K, Wingfield MJ, et al. Ophiostoma species, including Ophiostoma borealis sp. nov., infecting wounds of native broad-leaved trees in Norway. Cryptogam Mycol. 2010;31:285–303.

Conner RN, Miller OK Jr, Adkisson CS. Woodpecker dependence on trees infected by fungal rots. Wilson Bull. 1976;88:575–581.

Witt C. Characteristics of aspen infected with heartrot: implications for cavity-nesting birds. For Ecol Manage. 2010;260:1010–1016. https://doi.org/10.1016/j.foreco.2010.06.024

Rayner AD, Boddy L. Fungal decomposition of wood. Its biology and ecology. Chichester: John Wiley & Son; 1988.

Lindner DL, Vasaitis R, Kubátová A, Allmér J, Johannesson H, Banik MT, et al. Initial fungal colonizer affects mass loss and fungal community development in Picea abies logs 6 yr after inoculation. Fungal Ecol. 2011;4:449–460. https://doi.org/10.1016/j.funeco.2011.07.001

Jusino MA, Lindner DL, Cianchetti JC, Grisé AT, Brazee NJ, Walters JR. A minimally invasive method for sampling nest and roost cavities for fungi: a novel approach to identify the fungi associated with cavity-nesting birds. Acta Ornithol. 2014;49:233–242. https://doi.org/10.3161/173484714X687127

Hicks BR, Cobb FW Jr, Gersper PL. Isolation of Ceratocystis wageneri from forest soil with a selective medium. Phytopathology. 1980;70:880–883. https://doi.org/10.1094/Phyto-70-880

Kim JJ, Allen EA, Humble LM, Breuil C. Ophiostomatoid and basidiomycetous fungi associated with green, red and grey lodgepole pines after mountain pine beetle (Dendroctonus ponderosae) infestation. Can J For Res. 2005;35:274–284. https://doi.org/10.1139/x04-178

Ellis MB. Dematiaceous Hyphomycetes. Kew: Commonwealth Mycological Institute; 1971.

Barnett HL, Hunter BB. Illustrated genera of imperfect fungi. 3rd ed. Minneapolis, MN: Burgess Publishing Co.; 1972.

de Hoog GS. The genera Blastobotrys, Sporothrix, Calcarisporium and Calcarisporiella gen. nov. Stud Mycol. 1974;7:1–84.

Domsch KH, Gams W, Anderson TH. Compendium of soil fungi. London: Academic press; 1980.

Sutton BC. The Coelomycetes. Kew: Commonwealth Mycological Institute; 1980.

Upadhyay HP. Monograph of Ceratocystis and Ceratocystiopsis. Athens, GA: University of Georgia Press; 1981.

de Hoog GS, Guarro J, Gené J, Figueras MJ. Atlas of clinical fungi. 2nd ed. Utrecht: Centraalbureau voor Schimmelcultures; 2001.

Jankowiak R, Paluch J, Bilański P, Kołodziej Z. Fungi associated with dieback of Abies alba seedlings in naturally regenerating forest ecosystems. Fungal Ecol. 2016;24:61–69. https://doi.org/10.1016/j.funeco.2016.08.013

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–2729. https://doi.org/10.1093/molbev/mst197

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–780. https://doi.org/10.1093/molbev/mst010

Guindon S, Gascuel O. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol. 2003;52:696–704. https://doi.org/10.1080/10635150390235520

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772. https://doi.org/10.1038/nmeth.2109

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–321. https://doi.org/10.1093/sysbio/syq010

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180

Rambaut A, Drummond AJ. Tracer v1.4.2007 [cited 2018, April]. Available from http://beast.bio.ed.ac.uk/Tracer

Shannon CE, Weaver W. The mathematical theory of communication. Urbana, IL: University of Illinois Press; 1949.

Simpson EH. Measurement of species diversity. Nature. 1949;163:688. https://doi.org/10.1038/163688a0

Camargo JA. Must dominance increase with the number of subordinate species in competitive interactions? J Theor Biol. 1993;161:537–542. https://doi.org/10.1006/jtbi.1993.1072

Hammer O, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001;4(1):[9 p.].

Dix NJ, Webster J. Fungal ecology. New York, NY: Chapman & Hall; 1995. https://doi.org/10.1007/978-94-011-0693-1

Boddy L. Fungal community ecology and wood decomposition processes in angiosperms: from standing tree to complete decay of coarse woody debris. In: Jonsson BG, Kruys N, editors. Ecology of woody debris in boreal forests. Oxford: Blackwell; 2001. p. 43–56. (Ecological Bulletins; vol 49).

Boddy L, Heilmann-Clausen J. Basidiomycete community development in temperate angiosperm wood. In: Boddy L, Frankland JC, van West P, editors. Ecology of saprotrophic basidiomycetes. Amsterdam: Elsevier; 2008. p. 211–237. (British Mycological Society Symposia Series; vol 28). https://doi.org/10.1016/S0275-0287(08)80014-8

Kubartová A, Ottosson E, Dahlberg A, Stenlid J. Patterns of fungal communities among and within decaying logs, revealed by 454 sequencing. Mol Ecol. 2012;21:4514–4532. https://doi.org/10.1111/j.1365-294X.2012.05723.x

Domański S. Mała flora grzybów. Tom I. Basidiomycetes (Podstawczaki). Aphyllophorales (Bezblaszkowe). Cz. 1. Bondarzewiaceae (Bondarcewowate), Fistulinaceae (Ozorkowate), Ganodermataceae (Lakownicowate), Polyporaceae (Żagwiowate). Warszawa: PWN; 1974.

Domański S. Mała flora grzybów. Tom I. Basidiomycetes (Podstawczaki). Aphyllophorales (Bezblaszkowe). Cz. 2. Auriscalpiaceae, Bankeraceae, Clavicoronaceae, Coniophoraceae, Echinodontiaceae, Hericiaceae, Hydnaceae, Hymenochaetaceae, Lachnocladiaceae. Warszawa: PWN; 1975.

Sandoval-Denis M, Gené J, Sutton DA, Cano-Lira JF, de Hoog GS, Decock CA, et al. Redefining Microascus, Scopulariopsis and allied genera. Persoonia. 2016;36:1–36. https://doi.org/10.3767/003158516X688027

Sandoval-Denis M, Guarro J, Cano-Lira JF, Sutton DA, Wiederhold NP, de Hoog GS, et al. Phylogeny and taxonomic revision of Microascaceae with emphasis on synnematous fungi. Stud Mycol. 2016;83:193–233. https://doi.org/10.1016/j.simyco.2016.07.002

Woudenberg JHC, Sandoval-Denis M, Houbraken J, Seifert KA, Samson RA. Cephalotrichum and related synnematous fungi with notes on species from the built environment. Stud Mycol. 2017;88:137–159. https://doi.org/10.1016/j.simyco.2017.09.001

Rainer J, de Hoog GS. Molecular taxonomy and ecology of Pseudallescheria, Petriella and Scedosporium prolificans (Microascaceae) containing opportunistic agents on humans. Mycol Res. 2006;110:151–160. https://doi.org/10.1016/j.mycres.2005.08.003

Sandoval-Denis M, Sutton DA, Fothergill AW, Cano-Lira J, Gené J, Decock CA, et al. Scopulariopsis, a poorly known opportunistic fungus: spectrum of species in clinical samples and in vitro responses to antifungal drugs. J Clin Microbiol. 2013;51:3937–3943. https://doi.org/10.1128/JCM.01927-13

Lackner M, de Hoog GS, Yang L, Moreno LF, Ahmed SA, Andreas F, et al. Proposed nomenclature for Pseudallescheria, Scedosporium and related genera. Fungal Divers. 2014;67:1–10. https://doi.org/10.1007/s13225-014-0295-4

Jacobs K, Kirisitis T, Wingfield MJ. Taxonomic re-evaluation of three related species of Graphium, based on morphology, ecology and phylogeny. Mycologia. 2003;95:714–727. https://doi.org/10.2307/3761947

Geldenhuis MM, Roux J, Montenegro F, de Beer ZW, Wingfield MJ, Wingfield BD. Identification and pathogenicity of Graphium and Pesotum species from machete wounds on Schizolobium parahybum in Ecuador. Fungal Divers. 2004;15:137–151.

Paciura D, Zhou XD, de Beer ZW, Jacobs K, Wingfield MJ. Characterisation of synnematous bark beetle-associated fungi from China, including Graphium carbonarium sp. nov. Fungal Divers. 2010;40:75–88. https://doi.org/10.1007//s13225-009-0004-x

Piontelli E, Santa-Maria AM, Caretta G. Coprophilous fungi of the horse. Mycopathologia. 1981;74:89–105. https://doi.org/10.1007/BF01259464

Ibáñez-Álamo JD, Ruiz-Rodríguez M, Soler JJ. The mucous covering of fecal sacs prevents birds from infection with enteric bacteria. J Avian Biol. 2014;45:354–358. https://doi.org/10.1111/jav.00353

Lackner M, de Hoog GS. Parascedosporium and its relatives: phylogeny and ecological trends. IMA Fungus. 2011;21:39–48. https://doi.org/10.5598/imafungus.2011.02.01.07

de Beer ZW, Seifert KA, Wingfield MJ. The ophiostomatoid fungi: their dual position in the Sordariomycetes. In: Seifert KA, de Beer ZW, Wingfield MJ, editors. The ophiostomatoid fungi: expanding frontiers. Utrecht: CBS Fungal Diversity Center; 2013. p. 1–19. (CBS Biodiversity Series; vol 12).

Jankowiak R. Fungi associated with Ips typographus on Picea abies in southern Poland and their succession into the phloem and sapwood of beetle-infested trees and logs. For Pathol. 2005;35:37–55. https://doi.org/10.1111/j.1439-0329.2004.00395.x

Dowding P. Colonization of freshly bared pine sapwood surfaces by staining fungi. Transactions of the British Mycological Society. 1970;55:399–412. https://doi.org/10.1016/S0007-1536(70)80061-4

Käärik A. Succession of microorganisms during wood decay. In: Liese E, editor. Biological transformation of wood by microorganisms. Berlin: Springer; 1975. p. 39–51. https://doi.org/10.1007/978-3-642-85778-2_4

Herrera CS, Rossman AY, Samuels GJ, Chaverri P. Pseudocosmospora, a new genus to accommodate Cosmospora vilior and related species. Mycologia. 2013;105:1287–1305. https://doi.org/10.3852/12-395




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