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Patterns of distribution, abundance and composition of forest terrestrial orchids

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Abstract

Many terrestrial orchid species are known to grow in forest ecosystems, but the patterns of their diversity and habitat specialization have not been sufficiently explored. Niche parameters and factors influencing the distribution, abundance and composition of forest orchids in the central Balkans were investigated in the present study. Outlying mean index (OMI) analysis was used to explore ecological niches of orchids and environmental factors affecting the patterns of their distribution. Indicator species analysis was performed to identify species presenting strong affinity for specific forest and bedrock types. In addition, similarity profile analysis was applied to classify orchid taxa into meaningful groups, whereas the multi-response permutation procedure was used to analyse differences of orchid composition between forest types. Out of a total of 40 orchid species and subspecies analysed, 29 showed significant niche marginality. The first three axes of the OMI analysis explained 68.13% of total variability. Light, temperature, moisture, nitrogen and altitude were found to be the factors most effectively influencing the distribution and abundance of orchids. Seven orchids had statistically significant strong affinity for specific forest types, whereas eight orchids were statistically significantly correlated with specific bedrock types. Overall, six ecological groups of orchids were distinguished. The results suggest that specialist orchids occur at the extreme ends of the light, temperature, soil pH, moisture and altitude gradients. Moreover, most specialist orchid species were found from low to middle elevations. The results provide a useful basis for the successful design of strategies for the conservation of forest orchids.

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  • 27 October 2020

    In the original publication of the article, there were two minor errors identified. They are as follows:

References

  • Abernethy A (2002) Light regimes as a control of terrestrial orchid distribution in New Zealand. Dissertation, University of Canterbury

  • Acharya KP, Vetaas OR, Birks HJB (2011) Orchid species richness along Himalayan elevational gradients. J Biogeogr 38:1821–1833

    Google Scholar 

  • Averyanov L (1990) A review of the genus Dactylorhiza. In: Arditti J (ed) Orchid biology: reviews and perspectives. Timber Press Inc., Portland, pp 159–206

    Google Scholar 

  • Boulangeat I, Lavergne S, Van Es J, Garraud L, Thuiller W (2012) Niche breadth, rarity and ecological characteristics within a regional flora spanning large environmental gradients. J Biogeogr 39:204–214

    Google Scholar 

  • Braun-Blanquet J (1964) Pflanzensoziologie. Grundzüge der Vegetationskunde. Springer, Vienna

    Google Scholar 

  • Cavagnaro TR (2016) Soil moisture legacy effects: impacts on soil nutrients, plants and mycorrhizal responsiveness. Soil Biol Biochem 95:173–179

    CAS  Google Scholar 

  • Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201–217

    Google Scholar 

  • Chytrý M, Tichý L, Hennekens SM et al (2020) EUNIS Habitat Classification: expert system, characteristic species combinations and distribution maps of European habitats. Appl Veg Sci. https://doi.org/10.1111/avsc.12519

    Article  Google Scholar 

  • Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69

    Google Scholar 

  • De Caceres M, Jansen F (2014) Indicspecies: Studying the statistical relationship between species and groups of sites. http://cranr-project.org/web/packages/indicspecies/index.html (Version 1.6.7)

  • Delforge P (2006) Orchids of Europe, North Africa and the Middle East. A & C Black, London

    Google Scholar 

  • Diez JM, Pulliam HR (2007) Hierarchical analysis of species distribution and abundance across environmental gradients. Ecology 88:3144–3152

    PubMed  Google Scholar 

  • Djordjević V, Tsiftsis S, Lakušić D, Jovanović S, Stevanović V (2016a) Factors affecting the distribution and abundance of orchids in grasslands and herbaceous wetlands. Syst Biodivers 14:355–370

    Google Scholar 

  • Djordjević V, Tsiftsis S, Lakušić D, Stevanović V (2016b) Niche analysis of orchids of serpentine and non-serpentine areas: implications for conservation. Plant Biosyst 150:710–719

    Google Scholar 

  • Djordjević V, Tsiftsis S (2019) Patterns of orchid species richness and composition in relation to geological substrates. Wulfenia 26:1–21

    Google Scholar 

  • Dolédec S, Chessel D, Gimaret-Carpentier C (2000) Niche separation in community analysis: a new method. Ecology 81:2914–2927

    Google Scholar 

  • Dray S, Dufour AB, Chessel D (2007) The ade4 package-II: Two-table and K-table methods. R News 7:47–52

    Google Scholar 

  • Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Ellenberg H, Weber HE, Düll R et al (1991) Zeigerwerte von Pflanzen in Mitteleuropa. Scr Geobot 18:1–248

    Google Scholar 

  • Fayolle A, Engelbrecht B, Freycon V et al (2012) Geological substrates shape tree species and trait distributions in African moist forests. PLoS ONE 7:42381

    Google Scholar 

  • Fekete R, Löki V, Urgyán R et al (2019) Roadside verges and cemeteries: comparative analysis of anthropogenic orchid habitats in the Eastern Mediterranean. Ecol Evol 9:6655–6664

    PubMed  PubMed Central  Google Scholar 

  • Figura T, Weiser M, Ponert J (2020) Orchid seed sensitivity to nitrate reflects habitat preferences and soil nitrate content. Plant Biol 22:21–29

    CAS  PubMed  Google Scholar 

  • Fridley JD, Vandermast DB, Kuppinger DM, Manthey M, Peet RK (2007) Co-occurrence based assessment of habitat generalists and specialists: a new approach for the measurement of niche width. J Ecol 95:707–722

    Google Scholar 

  • Hágsater E, Dumont V (eds) (1996) Orchids: status, survey and conservation action plan. IUCN, Gland

    Google Scholar 

  • Hejcman M, Schellberg J, Pavlů V (2010) Dactylorhiza maculata, Platanthera bifolia and Listera ovata survive N application under P limitation. Acta Oecol 36:684–688

    Google Scholar 

  • Hemrová L, Kotilínek M, Konečná M et al (2019) Identification of drivers of landscape distribution of forest orchids using germination experiment and species distribution models. Oecologia 190:411–423

    PubMed  Google Scholar 

  • Hofmeister J, Hosek J, Modry M, Rolecek J (2009) The influence of light and nutrient availability on herb layer species richness in oak-dominated forests in central Bohemia. Plant Ecol 205:57–75

    Google Scholar 

  • Hrivnák R, Hrivnák M, Slezák M et al (2014) Distribution and eco-coenotic patterns of the forest orchid Epipactis pontica in Slovakia. Ann For Res 57:55–69

    Google Scholar 

  • Humphrey JW, Coombs EL (1997) Effects of forest management on understorey vegetation in a Pinus sylvestris L. plantation in NE Scotland. Bot J Scotl 49:479–488

    Google Scholar 

  • Hurskainen S, Jäkäläniemi A, Ramula S, Tuomi J (2017) Tree removal as a management strategy for the lady’s slipper orchid, a flagship species for herb-rich forest conservation. Forest Ecol Manag 406:12–18

    Google Scholar 

  • Jacquemyn H, Honnay O, Pailler T (2007) Range size variation, nestedness and species turnover of orchid species along an altitudinal gradient on Réunion Island: Implications for conservation. Biol Conserv 136:388–397

    Google Scholar 

  • Jacquemyn H, Brys R, Adriaens D et al (2009) Effects of population size and forest management ongenetic diversity and structure of the tuberous orchid Orchis mascula. Conserv Genet 10:161–168

    Google Scholar 

  • Jacquemyn H, Brys R, Jongejans E (2010) Size-dependent flowering and costs of reproduction affect population dynamics in a tuberous perennial woodland orchid. J Ecol 98:1204–1215

    Google Scholar 

  • Karadžić B (2018) Beech forests (order Fagetalia sylvaticae Pawlowski 1928) in Serbia. Bot Serb 42:91–107

    Google Scholar 

  • Kirca S, Kreutz KC, Çolak AH (2020) A biogeographical and ecological classification of orchids in Turkey. Phytocoenologia. https://doi.org/10.1127/phyto/2019/0292

    Article  Google Scholar 

  • Kojić M, Popović R, Karadžić B (1997) Vascular plants of Serbia as indicators of habitats. Institut za biološka istraživanja ‘Siniša Stanković’, Belgrade [in Serbian]

  • Kooijman AM (2010) Litter quality effects of beech and hornbeam on undergrowth species diversity in Luxembourg forests on limestone and decalcified marl. J Veg Sci 21:248–261

    Google Scholar 

  • Kostić O, Jarić S, Gajić G et al (2016) The effects of Douglas fir monoculture on stand characteristics in a zone of Montane beech forest. Arch Biol Sci 68:753–766

    Google Scholar 

  • Kotilínek M, Těšitelová T, Jersáková J (2015) Biological Flora of the British Isles: Neottia ovata. J Ecol 103:1354–1366

    Google Scholar 

  • Kotilínek M, Tatarenko I, Jersáková J (2018) Biological Flora of the British Isles: Neottia cordata. J Ecol 106:444–460

    Google Scholar 

  • Lõhmus A, Kull T (2011) Orchid abundance in hemiboreal forests: stand-scale effects of clearcutting, green-tree retention, and artificial drainage. Can J For Res 41:1352–1358

    Google Scholar 

  • Marinšek A, Čarni A, Šilc U, Manthey M (2015) What makes a plant species specialist in mixed broad-leaved deciduous forests? Plant Ecol 216:1469–1479

    Google Scholar 

  • McCormick MK, Jacquemyn H (2014) What constrains the distribution of orchid populations? New Phytol 202:392–400

    Google Scholar 

  • McCormick MK, Whigham DF, Canchani-Viruet A (2018) Mycorrhizal fungi affect orchid distribution and population dynamics. New Phytol 219:1207–1215

    PubMed  Google Scholar 

  • Milojić A (ed) (2015) Statistical Yearbook of Serbia 2015: Agriculture. Statistical Office of the Republic of Serbia, Belgrade. www.stat.gov.rs

  • Mölder A, Bernhardt-Römermann M, Schmidt W (2008) Herb-layer diversity in deciduous forests: raised by tree richness or beaten by beech? For Ecol Manag 256:272–281

    Google Scholar 

  • Mucina L, Bültmann H, Dierßen K et al (2016) Vegetation of Europe: hierarchical floristic classification system of plant, lichen, and algal communities. Appl Veg Sci 19:3–264

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R et al (2013) vegan: Community Ecology Package, R package version 2.0–7. http://CRAN.R-project.org/package=vegan

  • Pfeifer M, Passalacqua NG, Bartram S et al (2010) Conservation priorities differ at opposing species borders of a European orchid. Biol Conserv 143:2207–2220

    Google Scholar 

  • Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Rasmussen H (1995) Terrestrial orchids from seed to mycotrophic plant. Cambridge University Press, Cambridge

    Google Scholar 

  • Rewicz A, Jaskuła R, Rewicz T, Tończyk G (2017) Pollinator diversity and reproductive success of Epipactis helleborine (L.) Crantz (Orchidaceae) in anthropogenic and natural habitats. PeerJ 5:e3159

    PubMed  PubMed Central  Google Scholar 

  • Sagarin RD, Gaines SD (2002) The ‘abundant centre’distribution: to what extent is it a biogeographical rule? Ecol Lett 5:137–147

    Google Scholar 

  • Shefferson RP, Kull T, Tali K (2005) Adult whole-plant dormancy induced by stress in long-lived orchids. Ecology 86:3099–3104

    Google Scholar 

  • Slatyer RA, Hirst M, Sexton JP (2013) Niche breadth predicts geographical range size: a general ecological pattern. Ecol Lett 16:1104–1114

    PubMed  Google Scholar 

  • Somerfield PJ, Clarke KR (2013) Inverse analysis in non-parametric multivariate analyses: distinguishing of groups of associated species which covary coherently across samples. J Exp Mar Biol Ecol 449:261–273

    Google Scholar 

  • Štípková Z, Romportl D, Černocká V, Kindlmann P (2017) Factors associated with the distributions of orchids in the Jeseníky Mountains, Czech Republic. Eur J Environ Sci 7:135–145

    Google Scholar 

  • Štípková Z, Tsiftsis S, Kindlmann P (2020) Pollination mechanisms are driving orchid distribution in space. Sci Rep 10:850

    PubMed  PubMed Central  Google Scholar 

  • Swarts ND, Dixon KW (2009) Terrestrial orchid conservation in the age of extinction. Ann Bot 104:543–556

    PubMed  PubMed Central  Google Scholar 

  • Taylor L, Roberts DL (2011) Biological flora of the British Isles: Epipogium aphyllum Sw. J Ecol 99:878–890

    Google Scholar 

  • Thiele J, Schirmel J, Buchholz S (2018) Effectiveness of corridors varies among phytosociological plant groups and dispersal syndromes. PLoS ONE 13:e0199980

    PubMed  PubMed Central  Google Scholar 

  • Tinya F, Márialigeti S, Király I, Németh B, Ódor P (2009) The effect of light conditions on herbs, bryophytes and seedlings of temperate mixed forests in Őrség, Western Hungary. Plant Ecol 204:69–81

    Google Scholar 

  • Tranchida-Lombardo V, Cafasso D, Cristaudo A, Cozzolino S (2011) Phylogeographic patterns, genetic affinities and morphological differentiation between Epipactis helleborine and related lineages in a Mediterranean glacial refugium. Ann Bot 107:427–436

    PubMed  Google Scholar 

  • Tsiftsis S, Tsiripidis I, Karagiannakidou V, Alifragis D (2008) Niche analysis and conservation of the orchids of east Macedonia (NE Greece). Acta Oecol 33:27–35

    Google Scholar 

  • Tsiftsis S, Tsiripidis I, Karagiannakidou V (2009) Identifying areas of high importance for orchid conservation in east Macedonia (NE Greece). Biodivers Conserv 18:1765–1780

    Google Scholar 

  • Tsiftsis S, Tsiripidis I, Trigas P (2011) Identifying important areas for orchid conservation in Crete. Eur J Environ Sci 1:28–37

    Google Scholar 

  • Tsiftsis S, Tsiripidis I, Papaioannou A (2012) Ecology of orchid Goodyera repens in its southern distribution limits. Plant Biosyst 146:857–866

    Google Scholar 

  • Tsiftsis S, Djordjević V, Tsiripidis I (2019a) Neottia cordata (Orchidaceae) at its southernmost distribution border in Europe: threat status and effectiveness of Natura 2000 Network for its conservation. J Nat Conserv 48:27–35

    Google Scholar 

  • Tsiftsis S, Štípková Z, Kindlmann P (2019b) Role of way of life, latitude, elevation and climate on the richness and distribution of orchid species. Biodivers Conserv 28:75–96

    Google Scholar 

  • Vereecken NJ, Dafni A, Cozzolino S (2010) Pollination syndromes in Mediterranean orchids: implications for speciation, taxonomy and conservation. Bot Rev 76:220–240

    Google Scholar 

  • Vogt-Schilb H, Munoz F, Richard F, Schatz B (2015) Recent declines and range changes of orchids in Western Europe (France, Belgium and Luxembourg). Biol Conserv 190:133–141

    Google Scholar 

  • Waterman RJ, Bidartondo MI (2008) Deception above, deception below: linking pollination and mycorrhizal biology of orchids. J Exp Bot 59:1085–1096

    CAS  PubMed  Google Scholar 

  • WCSP (2020) World checklist of selected plant families. Royal Botanic Gardens, Kew. http://apps.kew.org/wcsp

    Google Scholar 

  • Whitaker D, Christman M (2014) Package “clustsig”: significant cluster analysis. R package v. 1.1. https://cran.r-project.org/

  • Zhang SB, Chen WY, Huang JL, Bi YF, Yang XF (2015) Orchid species richness along elevational and environmental gradients in Yunnan, China. PLoS ONE 10:e0142621

    PubMed  PubMed Central  Google Scholar 

  • Zhang S, Yang Y, Li J et al (2018) Physiological diversity of orchids. Plant Divers 40:196–208

    PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Yan Y, Tianb Y et al (2015b) Distribution and conservation of orchid species richness in China. Biol Conserv 181:64–72

    Google Scholar 

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Acknowledgements

This work was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (number 451-03-68/2020-14/200178). We are grateful to the Tara National Park, the Tourist Organization of Čačak and the Forest Estate ‘Golija’ Ivanjica for logistical field support. We thank two anonymous reviewers for their useful suggestions and comments on a previous version of the manuscript. We would also like to thank Mr. Raymond Dooley for proofreading the manuscript.

Funding

This work was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (number 451-03-68/2020-14/ 200178).

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Authors and Affiliations

  1. Faculty of Biology, Institute of Botany and Botanical Garden, University of Belgrade, Takovska 43, Belgrade, 11 000, Serbia

    Vladan Djordjević, Dmitar Lakušić, Slobodan Jovanović, Ksenija Jakovljević & Vladimir Stevanović

  2. Department of Forest and Natural Environment Sciences, International Hellenic University, P.O. Box 172, 1st km Dramas - Mikrochoriou, Drama, 66100, Greece

    Spyros Tsiftsis

  3. Academy of Science of the Czech Republic, Global Change Research Institute, Belidla 4a, Brno, 603 00, Czech Republic

    Spyros Tsiftsis

  4. Serbian Academy of Sciences and Arts, Kneza Mihaila 35, Belgrade, 11000, Serbia

    Vladimir Stevanović

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  1. Vladan Djordjević
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Correspondence to Vladan Djordjević.

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Djordjević, V., Tsiftsis, S., Lakušić, D. et al. Patterns of distribution, abundance and composition of forest terrestrial orchids. Biodivers Conserv 29, 4111–4134 (2020). https://doi.org/10.1007/s10531-020-02067-6

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