No CrossRef data available.
Article contents
EPIPHYTE RESPONSE TO WOODLAND HABITAT CONDITION ASSESSED USING COMMUNITY INDICATORS: A SIMPLIFIED METHOD FOR SCOTLAND’S TEMPERATE RAIN FOREST
Published online by Cambridge University Press: 09 June 2020
Abstract
National vegetation classification (NVC) has been widely applied as a framework for mapping and conserving plant species and community types. However, a limited availability of expertise has prevented NVCs from being developed and used in cryptogam-dominated systems, such as for temperate and boreal epiphyte communities. This study simplified a recent systematically sampled NVC, trialled for epiphyte communities in Scotland, by reducing the original list of 82 community indicators to 34 easily recognisable species (lichens, mosses and liverworts). These were subsequently sampled from woodland sites positioned in Scotland’s temperate rain forest zone. Sites were positioned among localities in less intensively managed landscapes (northwest Scotland) through to peri-urban environments (southern Scotland), grouping sites for each locality based on a contrast in woodland temporal continuity (ancient or recent). The richness and diversity of epiphyte community indicators were compared with easily measured variables reflecting stand heterogeneity or ecological stability, and woodland temporal continuity, with air pollution as a covariable. Richness and diversity were significantly explained by the ecological stability of woodland stands, heterogeneity of the light environment, and nitrogen pollution. This demonstrates a tool that can be deployed by the non-specialist, with appropriate training, to quantify the condition of a woodland stand through consequences for its epiphytes in globally important temperate rain forest. The pattern of richness and diversity was consistent with the co-occurrence of particular indicator species, which represent the range of epiphyte community types supported by a woodland.
- Type
- Articles
- Information
- Copyright
- © Trustees of the Royal Botanic Garden Edinburgh (2020)
References
Air Pollution Information System (no date). Online. Available: Air Pollution Information System http://www.apis.ac.uk/
Google Scholar
Anonymous (2008). Ancient Tree Guide 4: What are Ancient, Veteran and Other Trees of Special Interest? Grantham: Woodland Trust and Ancient Tree Forum.Google Scholar
Aragón, G., Martínez, I., Izquierdo, P., Belinchón, R. & Escudero, A. (2010). Effects of forest management on epiphytic lichen diversity in Mediterranean forests. Appl. Veg. Sci. 13(2): 183–194.CrossRefGoogle Scholar
Averis, A. M., Averis, A. B. G., Birks, H. J. B., Horsfield, D., Thompson, D. B. A. & Yeo, M. J. M. (2004). An Ilustrated Guide to British Upland Vegetation. Peterborough: Joint Nature Conservation Committee.Google Scholar
Barkman, J. J. (1958). Phytosociology and Ecology of Cryptogamic Epiphytes. Assen: Van Corcum & Comp.Google Scholar
Bauhus, J., Puettmann, K. & Messier, C. (2009). Silviculture for old-growth attributes. Forest Ecol. Managem. 258(4): 525–537.CrossRefGoogle Scholar
Bergmeier, E., Petermann, J. & Schröder, E. (2010). Geobotanical survey of wood-pasture habitats in Europe: diversity, threats and conservation. Biodivers. & Conservation 19: 2995–3014.CrossRefGoogle Scholar
Coppins, B. J. & Coppins, A. M. (2005). Lichens – the biodiversity value of western woodlands. Bot. J. Scotland 57: 141–153.CrossRefGoogle Scholar
Coppins, S. & Coppins, B. J. (2012). Atlantic Hazel. Scotland’s Special Woodlands. Kilmartin: Atlantic Hazel Action Group.Google Scholar
Corsie, E. I., Harrold, P. & Yahr, R. (2019). No combination of morphological, ecological or chemical characters can reliably diagnose species in the Parmelia saxatilis aggregate in Scotland. Lichenologist 51(2): 107–121.CrossRefGoogle Scholar
Dias, E., Elias, R. B. & Nunes, V. (2004). Vegetation mapping and nature conservation: a case study in Terceira Island (Azores). Biodivers. & Conservation 13: 1519–1539.CrossRefGoogle Scholar
Duigan, C., Kovach, W. & Palmer, M. (2007). Vegetation communities of British lakes: a revised classification scheme for conservation. Aquat. Conserv. 17(2): 147–173.CrossRefGoogle Scholar
Elbert, W., Weber, B., Burrows, S., Steinkamp, J., Büdel, B., Andreae, M. A. & Pöschl, U. (2012). Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nature Geosci. 5: 459–462.CrossRefGoogle Scholar
Ellis, C. J. (2016). Oceanic and temperate rainforest climates and their epiphyte indicators in Britain. Ecol. Indicators 70: 125–133.CrossRefGoogle Scholar
Ellis, C. J. & Coppins, B. J. (2017). Taxonomic survey compared to ecological sampling: are the results consistent for woodland epiphytes? Lichenologist 49: 141–155.CrossRefGoogle Scholar
Ellis, C. J., Yahr, R. & Coppins, B. J. (2009). Local extent of old-growth woodland modifies epiphyte response to climate change. J. Biogeogr. 36: 302–313.Google Scholar
Ellis, C. J., Eaton, S., Theodoropoulos, M., Coppins, B. J., Seaward, M. R. D. & Simkin, J. (2014). Response of epiphytic lichens to 21st century climate change and tree disease scenarios. Biol. Conservation 180: 153–164.CrossRefGoogle Scholar
Ellis, C. J., Eaton, S., Theodoropoulos, M. & Elliott, K. (2015a). Epiphyte Communities and Indicator Species. An Ecological Guide for Scotland’s Woodlands. Edinburgh: Royal Botanic Garden Edinburgh.Google Scholar
Ellis, C. J., Eaton, S., Theodoropoulos, M., Coppins, B. J., Seaward, M. R. D. & Simkin, J. (2015b). Lichen Epiphyte Scenarios. A Toolkit of Climate and Woodland Change for the 21st Century. Edinburgh: Royal Botanic Garden Edinburgh.Google Scholar
Englund, S. R., O’Brien, J. J. & Clark, D. B. (2000). Evaluation of digital and film hemispherical photography and spherical densiometry for measuring forest light environments. Canad. J. Forest Res. 30: 1999–2005.CrossRefGoogle Scholar
Fay, N. (2007). Defining and Surveying Veteran and Ancient Trees. Peterborough: UK Biodiversity Action Plan.Google Scholar
Fowler, D., O’Donoghue, M., Muller, J. B. A., Smith, R. I., Dragosits, U., Skiba, U., Sutton, M. A. & Brimblecombe, P. (2004). A chronology of nitrogen deposition in the UK between 1900 and 2004. Water Air Soil Pollut. 4: 9–23.CrossRefGoogle Scholar
Gilbert, O. L. (1970). A biological scale for the estimation of sulphur dioxide pollution. New Phytol. 69: 629–634.CrossRefGoogle Scholar
Gilbert, O. L. (1974). An air pollution survey by school children. Environm. Pollut. 6: 175–180.CrossRefGoogle Scholar
Giordani, P., Brunialti, G., Benesperi, R., Rizzi, G., Frati, L. & Modenesi, P. (2009). Rapid biodiversity assessment in lichen diversity surveys: implications for quality assurance. J. Environm. Monit. 11: 730–735.CrossRefGoogle ScholarPubMed
Green, T. G. A., Kilian, E. & Lange, O. L. (1991).
Pseudocyphellaria dissimilis: a desiccation-sensitive, highly shade-adapted lichen from New Zealand. Oecologia 85: 498–450.CrossRefGoogle ScholarPubMed
Gunnarson, B., Hake, M. & Hultengren, S. (2004). A functional relationship between species richness of spiders and lichens in spruce. Biodivers. & Conservation 13: 685–693.CrossRefGoogle Scholar
Hawksworth, D. L. & Rose, F. (1970). Qualitative scale for estimating sulphur dioxide air pollution in England and Wales using epiphytic lichens. Nature 227: 145–148.CrossRefGoogle ScholarPubMed
James, P. W., Hawksworth, D. H. & Rose, F. (1977). Lichen communities in the British Isles: a preliminary conspectus. In: Seaward, M. R. D. (ed.) Lichen Ecology, pp. 295–413. London: Academic Press.Google Scholar
Jennings, M. D., Faber-Langendoen, D., Loucks, O. L., Peet, R. K. & Roberts, D. (2009). Standards for associations and alliances of the U.S. National Vegetation Classification. Ecol. Monogr. 79: 173–199.CrossRefGoogle Scholar
Johansson, O., Palmqvist, K. & Olofsson, J. (2012). Nitrogen deposition drives lichen community changes through differential species responses. Global Change Biol. 18: 2626–2635.CrossRefGoogle Scholar
Király, I., Nascimbene, J. & Ódor, P. (2013). Factors influencing epiphytic bryophyte and lichen species richness at different spatial scales in managed temperate forests. Biodivers. & Conservation 22: 209–223.CrossRefGoogle Scholar
Krebs, C. J. (1999). Ecological Methodology. Menlo Park, California: Benjamin Cummings.Google Scholar
Lemmon, P. E. (1956). A spherical densiometer for estimating forest overstory density. Forest Sci. 2: 314–320.Google Scholar
Leppik, E., Jüriado, I. & Liira, J. (2011). Changes in stand structure due to the cessation of traditional land use in wooded meadows impoverish epiphytic lichen communities. Lichenologist 43: 257–274.CrossRefGoogle Scholar
Lesica, P., McCune, B., Cooper, S. V. & Hong, W. S. (1991). Differences in lichen and bryophyte communities between old-growth and managed second-growth forests in the Swan Valley, Montana. Canad. J. Bot. 69: 1745–1755.CrossRefGoogle Scholar
Lindenmayer, D. B. (2017). Conserving large old trees as small natural features. Biol. Conservation 211: 51–59.CrossRefGoogle Scholar
Lindenmayer, D. B., Laurance, W. F. & Franklin, J. F. (2012). Global decline in large old trees. Science 338: 1305–1306.CrossRefGoogle ScholarPubMed
Lindenmayer, D. B., Laurance, W. F., Franklin, J. F., Likens, G. E., Banks, S. C., Blanchard, W., Gibbons, P., Ikin, K., Blair, D., McBurney, L., Manning, A. D. & Stein, J. A. R. (2014). New policies for old trees: averting a global crisis in a keystone ecological structure. Conserv. Lett. 7: 61–69.CrossRefGoogle Scholar
Lõhmus, A., Lõhmus, P. & Vellak, K. (2007). Substratum diversity explains landscape-scale covariation in the species-richness of bryophytes and lichens. Biol. Conservation 135: 405–414.CrossRefGoogle Scholar
Marmor, L., Tõrra, T., Saag, L. & Randlane, T. (2012). Species richness of epiphytic lichens in coniferous forests: the effect of canopy openness. Ann. Bot. Fenn. 49: 352–358.CrossRefGoogle Scholar
McCune, B. (2000). Lichen communities as indicators of forest health. Bryologist 103: 353–356.CrossRefGoogle Scholar
McCune, B. & Grace, J. B. (2002). Analysis of Ecological Communities. Gleneden Beach, Oregon: MjM Software Design.Google Scholar
McCune, B. & Mefford, M. J. (2011). PC-ORD. Multivariate Analysis of Ecological Data. Version 6. Gleneden Beach, Oregon: MjM Software.Google Scholar
McCune, B., Dey, J. P., Peck, J. E., Cassell, D., Heiman, K., Will-Wolf, S. & Neitlich, P. N. (1997). Repeatability of community data: species richness versus gradient scores in large-scale lichen studies. Bryologist 100: 40–46.CrossRefGoogle Scholar
McMurray, J. A., Roberts, D. W. & Geiser, L. H. (2015). Epiphytic lichen indication of nitrogen deposition and climate in the northern rocky mountains, USA. Ecol. Indicators 49: 154–161.CrossRefGoogle Scholar
Mežaka, A., Brūmelis, G. & Piterāns, A. (2008). The distribution of epiphytic bryophyte and lichen species in relation to phorophyte characters in Latvian natural old-growth broad leaved forests. Folia Cryptog. Estonica 44: 89–99.Google Scholar
Michel, A. K. & Winter, S. (2009). Tree microhabitat structures as indicators of biodiversity in Douglas-fir forests of different stand ages and management histories in the Pacific Northwest, U.S.A. Forest Ecol. Managem. 257: 1453–1464.CrossRefGoogle Scholar
Mucina, L., Schaminée, J. H. J. & Rodwell, J. S. (2000). Common data standards for recording relevés in field survey for vegetation classification. J. Veg. Sci. 11: 769–772.CrossRefGoogle Scholar
Nascimbene, J., Marini, L. & Ódor, P. (2012). Drivers of lichen species richness at multiple spatial scales in temperate forests. Pl. Ecol. Diversity 5: 355–363.CrossRefGoogle Scholar
Negtap (2001). Transboundary Air Pollution: Acidification, Eutrophication and Ground-Level Ozone in the UK. Edinburgh: Centre for Ecology and Hydrology.Google Scholar
Paletto, A. & Tosi, V. (2009). Forest canopy cover and canopy closure: comparison of assessment techniques. Eur. J. Forest Res. 128: 265–272.CrossRefGoogle Scholar
Palmqvist, K. & Sundberg, B. (2000). Light use efficiency of dry matter gain in five macro-lichens: relative impact of microclimate conditions and species-specific traits. Pl. Cell Environm. 23: 1–14.CrossRefGoogle Scholar
Paltto, H., Nordberg, A., Nordén, B. & Snäll, T. (2011). Development of secondary woodland in oak wood pastures reduces the richness of rare epiphytic lichens. PLoS ONE 6: e24675.CrossRefGoogle ScholarPubMed
Petterson, R. B., Ball, J. P., Renhorn, K.-E., Esseen, P.-A. & Sjöberg, K. (1995). Invertebrate communities in boreal forest canopies as influenced by forestry and lichens with implications for passerine birds. Biol. Conservation 74: 57–63.CrossRefGoogle Scholar
Porada, P., Weber, B., Elbert, W., Pöschl, U. & Kleidon, A. (2014). Estmating impacts of lichens and bryophytes on global biogeochemical cycles. Global Biogeochem. Cycles 28: 71–85.CrossRefGoogle Scholar
Pypker, T. G., Unsworth, M. H. & Bond, B. J. (2006a). The role of epiphytes in rainfall interception by forests in the Pacific Northwest. II. Field measurements at the branch and canopy scale. Canad. J. Forest Res. 36: 819–832.CrossRefGoogle Scholar
Pypker, T. G., Unsworth, M. H. & Bond, B. J. (2006b). The role of epiphytes in rainfall interception by forests in the Pacific Northwest. I. Laboratory measurements of water storage. Canad. J. Forest Res. 36: 809–818.CrossRefGoogle Scholar
Reiners, W. A. & Olson, R. K. (1984). Effects of canopy components on throughfall chemistry: an experimental approach. Oecologia 63: 320–330.CrossRefGoogle Scholar
Roberts, A. J., Russel, C., Walker, G. J. & Kirby, K. J. (1992). Regional variation in the origin, extent and composition of Scottish woodland. Bot. J. Scotland 46: 167–189.CrossRefGoogle Scholar
Rodwell, J. S. (ed.) (1991) British Plant Communities, Volume 1. Woodland and Scrub. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Rodwell, J. S., Mucina, L., Pignatti, S., Schaminée, J. H. J. & Chytrý, M. (1997). European vegetation survey: the context of the case studies. Folia Geobot. 32: 113–115.CrossRefGoogle Scholar
Rose, F. (1976). Lichenological indicators of age and environmental continuity in woodlands. In: Brown, D. H., Hawksworth, D. L. & Bailey, R. H. (eds) Lichenology: Progress and Problems, pp. 279–307. London: Academic Press.Google Scholar
RoTAP (2012). Review of Transboundary Air Pollution: Acidification, Eutrophication, Ground Level Ozone and Heavy Metals in the UK. Edinburgh: Centre for Ecology and Hydrology.Google Scholar
Seaward, M. R. D. (1998). Time–space analysis of the British lichen flora, with particular reference to air quality surveys. Folia Cryptog. Estonica 32: 85–96.Google Scholar
Seed, L., Wolseley, P., Gosling, L., Davies, L. & Power, S. A. (2013). Modelling relationships between lichen bioindicators, air quality and climate on a national scale: results from the UK OPAL survey. Environm. Pollut. 182: 437–447.CrossRefGoogle ScholarPubMed
Selva, S. B. (1994). Lichen diversity and stand continuity in the northern hardwoods and spruce-fir forests of northern New England and western New Brunswick. Bryologist 97(4): 424–429.CrossRefGoogle Scholar
Sillett, S. C., McCune, B., Peck, J. E. & Rambo, T. R. (2000). Four years of epiphyte colonization in Douglas-fir forest canopies. Bryologist 103(4): 661–669.CrossRefGoogle Scholar
Smout, T. C. (2005). Oak as a commercial crop in the eighteenth and nineteenth centuries. Bot. J. Scotland 57(1–2): 107–114.CrossRefGoogle Scholar
Smout, T. C., Macdonald, A. R. & Watson, F. (2007). A History of the Native Woodlands of Scotland, 1500–1920. Edinburgh: Edinburgh University Press.Google Scholar
Solhaug, K. A. & Gauslaa, Y. (1996). Parietin, a photoprotective secondary product of the lichen Xanthoria parietina
. Oecologia 108(3): 412–418.CrossRefGoogle ScholarPubMed
Spier, L., van Dobben, H. & van Dort, K. (2010). Is bark pH more important than tree species in determining the composition of nitrophytic or acidophytic lichen floras? Environm. Pollut. 158(12): 3607–3611.CrossRefGoogle ScholarPubMed
Stein, A., Gerstner, K. & Kreft, H. (2014). Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol. Letters 17(7): 866–880.CrossRefGoogle ScholarPubMed
Stubbs, C. S. (1989). Patterns of distribution and abundance of corticolous lichens and their invertebrate associates on Quercus rubra in Maine. Bryologist 92(4): 453–460.CrossRefGoogle Scholar
Tansley, A. G. (1913). Review: a universal classification of plant-communities. J. Ecol. 1(1): 27–42.CrossRefGoogle Scholar
Tregidgo, D. J., West, S. E. & Ashmore, M. R. (2013). Can citizen science produce good science? Testing the OPAL Air Survey methodology, using lichens as indicators of nitrogenous pollution. Environm. Pollut. 182: 448–451.CrossRefGoogle ScholarPubMed
Tripp, E. A., Lendemer, J. C. & McCain, C. M. (2019). Habitat quality and disturbance drive lichen species richness in a temperate biodiversity hotspot. Oecologia 190: 445–457.CrossRefGoogle Scholar
Van Herk, C. M., Mathijssen-Spiekman, E. A. M. & de Zwart, D. (2003). Long distance nitrogen air pollution effects on lichens in Europe. Lichenologist 35(4): 347–359.CrossRefGoogle Scholar
Van Stan, J. T. & Pypker, T. G. (2015). A review and evaluation of forest canopy epiphyte roles in the partitioning and chemical alteration of precipitation. Sci. Total Environm. 536: 813–824.CrossRefGoogle ScholarPubMed
Vestreng, V., Myhre, G., Fagerli, H., Reis, S. & Tarrasón, L. (2007). Twenty-five years of continuous sulphur dioxide emission reduction in Europe. Atmos. Chem. Phys. 7: 3663–3681.CrossRefGoogle Scholar
Vondrák, J., Malíček, J., Palice, Z., Coppins, B., Kukwa, M., Czarnota, P., Sanderson, N. & Acton, A. (2016). Methods for obtaining more complete species lists in surveys of lichen diversity. Nordic J. Bot. 34(5): 619–626.CrossRefGoogle Scholar
Walker, G. J. & Kirby, K. J. (1989). Inventories of Ancient, Long-established and Semi-natural Woodland for Scotland. Research & Survey in Nature Conservation No. 22. Peterborough: Nature Conservancy Council.Google Scholar
Whittet, R. & Ellis, C. J. (2013). Critical tests for lichen indicators of woodland ecological continuity. Biol. Conservation 168: 19–23.CrossRefGoogle Scholar
Whittet, R., Hope, J. & Ellis, C. J. (2015). Open structured woodland and the ecological interpretation of Scotland’s Ancient Woodland Inventory. Scott. Geogr. J. 131(2): 67–77.CrossRefGoogle Scholar
Williams, L. & Ellis, C. J. (2018). Ecological constraints to ‘old-growth’ lichen indicators: niche specialism or dispersal limitation? Fungal Ecol. 34: 20–27.CrossRefGoogle Scholar
Wolseley, P. A., James, P. W., Theobald, M. R. & Sutton, M. A. (2006). Detecting changes in epiphytic lichen communities at sites affected by atmospheric ammonia from agricultural sources. Lichenologist 38(2): 161–176.CrossRefGoogle Scholar
Woodin, S. J. (1989). Environmental effects of air pollution in Britain. J. Appl. Ecol. 26(3): 749–761.CrossRefGoogle Scholar