Biodiversity and Conservation

, Volume 27, Issue 9, pp 2363–2377 | Cite as

Quantifying the anthropocene loss of bioindicators for an early industrial region: an equitable baseline for biodiversity restoration

  • Christopher J. Ellis
  • Rebecca Yahr
  • Brian J. Coppins
Original Paper
Part of the following topical collections:
  1. Urban biodiversity


Directly observed biodiversity data have a limited temporal span of c. 100–150 years. Consequently, for a region such as temperate Western Europe, our knowledge of species distributions is restricted to a period impacted by the process of massive industrialisation. There is a danger of shifted baselines in terms of conservation policy and targets. Here we present a novel source of high resolution archaeobotanical information for lichen epiphyte bioindicators; these data can reconstruct species distributions for the pre-industrial European landscape. We compare these historic records to a species’ post-industrial distribution and environmental response, quantifying the spatial trend and causes of biodiversity loss. The results indicate regional extinction rates of c. 76% in response to habitat loss and industrial pollution. We propose pre-industrial baselines that would better represent biodiversity restoration for temperate regions (net gain), and which would be equitable with advocacy for species and habitat protection in the present-day tropics (no net loss).


Anthropocene Archaeobotany Bioindicators Net biodiversity gain Restoration ecology Shifting baselines 



The authors wish to thank David Andrews, Roger Champion, John Dallimore, Richard Harris, Martin Higgins, Joe Thompson, Dorothy Treasure and Nigel Walker for providing invaluable assistance interpreting dates of vernacular buildings, and the National Trust at Holnicote Estate for arranging access in Exmoor. We especially thank all the individual owners and tenants who allowed us to access their homes and barns for this research. The work was funded by a grant to CJE from The Leverhulme Trust, ‘Britain’s Lost Biodiversity’ (# F/00 771/B). An original manuscript was improved by the comments of two reviewers.

Supplementary material

10531_2018_1541_MOESM1_ESM.pdf (336 kb)
Supplementary material 1 (PDF 336 kb)


  1. Ahrends A, Burgess ND, Milledge SAH, Bulling MT, Fisher B, Smart JCR, Clarke GP, Mhoro BE, Lewis SL (2010) Predictable waves of sequential forest degradation and biodiversity loss spreading from an African city. Proc Natl Acad Sci 107:14556–14561PubMedPubMedCentralGoogle Scholar
  2. Bauhus J, Puettmann K, Messier C (2009) Silviculture for old-growth attributes. For Ecol Manage 258:525–537Google Scholar
  3. Berglund H, Jonsson BG (2005) Verifying an extinction debt among lichens and fungi in northern Swedish boreal forests. Conserv Biol 19:338–348Google Scholar
  4. Bull JW, Brownlie S (2017) The transition from no net loss to a net gain of biodiversity is far from trivial. Oryx 5:53–59Google Scholar
  5. Burgess ND, Clarke GP, Rodgers WA (1998) Coastal forests of eastern Africa: status, endemism patterns and their potential causes. Biol J Lin Soc 64:337–367Google Scholar
  6. Butchart SHM, Walpole M, Collen B, van Strien A, Scharlemann JPW, Almond REA, Baillie JEM, Bomhard B, Brown C, Bruno J, Carpenter KE, Carr GM, Chanson J, Chenery AM, Csirke J, Davidson NC, Dentener F, Foster M, Galli A, Galloway JN, Genovesi P, Gregory RD, Hockings M, Kapos V, Lamarque JF, Leverington F, Loh J, McGeoch MA, McRae L, Minasyan A, Morcillo MH, Oldfield TEE, Pauly D, Quader S, Ravenga C, Sauer JR, Skolnik B, Spear D, Stanwell-Smith D, Stuart SN, Symes A, Tierney M, Tyrrell TD, Vié JC, Watson R (2010) Global biodiversity: indicators of decline. Science 328:1164–1168PubMedGoogle Scholar
  7. Chandra A, Idrisova A (2011) Convention on Biological Diversity: a review of national challenges and opportunities for implementation. Biodivers Conserv 20:3295–3316Google Scholar
  8. Coppins AM, Coppins BJ (2003) Atlantic hazelwoods—a neglected habitat? Bot J Scotl 55:149–160Google Scholar
  9. Coppins BJ, Coppins AM (2005) Lichens—the biodiversity value of western woodlands. Bot J Scotl 57:141–153Google Scholar
  10. Coppins BJ, Coppins AM (2006) The lichens of Scottish native pinewoods. Forestry 79:249–259Google Scholar
  11. Crutzen PJ, Steffen W (2003) How long have we been in the anthropocene era? Climatic Change 61:251–257Google Scholar
  12. Currie CRJ (1983) Timber supply and timber building in a Sussex parish. Vernac Archit 14:52–54Google Scholar
  13. Das P (2005) Hugh Cleghorn and forest conservancy in India. Environ Hist 11:55–82Google Scholar
  14. DellaSala DA (2011) Temperate and boreal rainforests of the world: ecology and conservation. Island Press, WashingtonGoogle Scholar
  15. Dettki H, Klintberg P, Esseen P-A (2000) Are epiphytic lichens in young forests limited by local dispersal? Écoscience 7:317–325Google Scholar
  16. Dollar D, Kraay A (2004) Trade, growth and poverty. Econ J 114:22–49Google Scholar
  17. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57Google Scholar
  18. Ellis CJ (2016) Oceanic and temperate rainforest climates and their epiphyte indicators in Britain. Ecol Ind 70:125–133Google Scholar
  19. Ellis CJ (2017) When is translocation required for the population recovery of old-growth epiphytes in a reforests landscape? Restor Ecol (In press)Google Scholar
  20. Ellis CJ, Coppins BJ (2007) 19th Century woodland structure controls stand-scale epiphyte diversity in present-day Scotland. Divers Distrib 13:84–91Google Scholar
  21. Ellis CJ, Coppins BJ, Dawson TP, Seaward MRD (2007) Response of British lichens to climate change scenarios: trends and uncertainties in the projected impact for contrasting biogeographic groups. Biol Cons 140:217–235Google Scholar
  22. Ellis CJ, Eaton S, Theodoropoulos M, Coppins BJ, Seaward MRD, Simkin J (2014) Response of epiphytic lichens to 21st Century climate change and tree disease scenarios. Biol Cons 180:153–164Google Scholar
  23. Ellis CJ, Eaton S, Theodoropoulos M, Coppins BJ, Seaward MRD, Simkin J (2015) Lichen epiphyte scenarios a toolkit of climate and woodland change for the 21st century. Royal Botanic Garden Edinburgh, EdinburghGoogle Scholar
  24. Falkner R (2012) Global environmentalism and the greening of international society. Int Aff 88:503–522Google Scholar
  25. Firebaugh G (2000) The trend in between-nation income inequality. Ann Rev Soc 26:323–339Google Scholar
  26. Fisher B, Christopher T (2007) Poverty and biodiversity: measuring the overlap of human poverty and the biodiversity hotspots. Ecol Econ 62:93–101Google Scholar
  27. Fowler D, O’Donoghue M, Muller JBA, Smith RI, Dragosits U, Skiba U, Sutton MA, Brimblecombe P (2004) A chronology of nitrogen deposition in the UK between 1900 and 2004. Water Air Soil Pollut 4:9–23Google Scholar
  28. Fritz O, Heilmann-Clausen J (2010) Rot holes create key microhabitats for epiphytic lichens and bryophytes on beech (Fagus sylvatica). Biol Cons 143:1008–1016Google Scholar
  29. Fyfe RM, Woodbridge J, Roberts AJ (2015) From forest to farmland: pollen-inferred land cover change across Europe using the pseudobiomization approach. Glob Change Biol 21:1197–1212Google Scholar
  30. Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227PubMedGoogle Scholar
  31. Gilbert OL (1965) Lichens as indicators of air pollution in the Tyne Valley. In: Goodman GT, Edwards RW, Lambert JM (eds) Ecology and the Industrial Society. Blackwell, Oxford, pp 35–47Google Scholar
  32. Gilbert OL (1970) A biological scale for the estimation of sulphur dioxide pollution. New Phytol 69:629–634Google Scholar
  33. Goward T (1994) Notes on old growth-dependent epiphytic macrolichens in inland British Columbia Canada. Acta Botanica Fennica 150:31–38Google Scholar
  34. Griggs D, Stafford-Smith M, Gaffney O, Rockström J, Öhman MC, Shyamsundar P, Steffen W, Glaser G, Kanie N, Noble I (2013) Sustainable development goals for people and planet. Nature 495:305–307PubMedGoogle Scholar
  35. Groves C (2000) Belarus to Bexley and beyond: dendrochronology and dendroprovenancing of conifer timbers. Vernac Archit 31:59–66Google Scholar
  36. Haneca K, Čufar K, Beeckman H (2009) Oaks tree-rings and wooden cultural heritage: a review of the main characteristics and applications of oak dendrochronology in Europe. J Archaeol Sci 36:1–11Google Scholar
  37. Harris R (1993) Discovering Timber-Framed Buildings. Osprey Publishing, Princes RisboroughGoogle Scholar
  38. Hawksworth DL (1971) Lichens as litmus for air pollution: a historical review. Int J Environ Stud 1:281–296Google Scholar
  39. Hawksworth DH, McManus PM (1989) Lichen recolonization in London under conditions of rapidly fally sulphur dioxide levels, and the concept of zone skipping. Bot J Linn Soc 100:99–109Google Scholar
  40. Hawksworth DL, Rose F (1970) Qualitative scale for estimating sulphur dioxide air pollution in England and Wales using epiphytic lichens. Nature 227:145–148PubMedGoogle Scholar
  41. Hewett CA (1980) English historic carpentry. Phillimore, ChichesterGoogle Scholar
  42. Hill DJ (1971) Experimental study of the effect of sulphite in lichens with reference to atmospheric pollution. New Phytol 70:831–836Google Scholar
  43. Johansson V, Ranius T, Snäll T (2013a) Epiphyte metapopulation persistence after drastic habitat decline and low tree regeneration: time-lags and effects of conservation actions. J Appl Ecol 50:414–422Google Scholar
  44. Johansson V, Snäll T, Ranius T (2013b) Estimates of connectivity reveal non-equilibrium epiphyte occurrence patterns almost 180 years after habitat decline. Oecologia 172:607–615PubMedGoogle Scholar
  45. Kangalawe RYM, Noe C (2012) Biodiversity conservation and poverty alleviation in Namtumbo District Tanzania. Agr Ecosyst Environ 162:90–100Google Scholar
  46. Kirk JC (2004) Butt’s Cottage Kirdford: the conversion of trees to timber in the rural Sussex Weald. Vernac Archit 35:12–20Google Scholar
  47. Kummu M, Varis O (2010) The world by latitudes: a global analysis of human population development and environment across the north-south axis over the past half century. Appl Geogr 31:495–507Google Scholar
  48. 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. The Lichenol 43:257–274Google Scholar
  49. Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:778–789Google Scholar
  50. Lõhmus A, Lõhmus P (2011) Old-forest species: the importance of specific substrata vs stand continuity in the case of Calicioid fungi. Silva Fennica 45:1015–1039Google Scholar
  51. Lõhmus A, Runnel K (2014) Ash dieback can rapidly eradicate isolated epiphyte populations in production forests: a case study. Biol Cons 169:185–188Google Scholar
  52. Maddison A (1983) A comparison of levels of GDP per capita in developed and developing countries, 1700-1980. J Econ Hist 43:27–41Google Scholar
  53. Magurran AE, Baillie SR, Buckland ST, Dick JM, Elston DA, Scott EM, Smith RI, Somefield PJ, Watt AD (2010) Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. Trends Ecol Evol 25:574–582PubMedGoogle Scholar
  54. Mathias P (1983) The First Industrial Nation: The Economic History of Britain 1700-1914. Routledge, LondonGoogle Scholar
  55. McShane TO, Hirsch PD, Trung TC, Songorwa AN, Kinzig A, Monteferri B, Mutekanga D, van Thang H, Dammert JD, Pulgar-Vidal M, Welch-Devine M, Brosius JP, Coppolillo P, O’Connor S (2011) Hard choices: making trade-offs between biodiversity conservation and human well-being. Biol Cons 144:966–972Google Scholar
  56. Meeson B (2012) Structural trends in English Medieval buildings: new insights from dendrochronology. Vernac Archit 43:58–75Google Scholar
  57. Mihoub J-B, Henle K, Titeux N, Brotons L, Brummit NA, Schmeller DS (2017) Setting temporal baselines for biodiversity: the limits of available monitoring data for capturing the full effect of anthropogenic pressures. Sci Rep 7:41591PubMedPubMedCentralGoogle Scholar
  58. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedGoogle Scholar
  59. Ohlson M, Söderström L, Hörnberg G, Zackrisson O, Hermansson J (1997) Habitat qualities versus long-term continuity as determinants of biodiversity in boreal old-growth swamp forests. Biol Cons 81:221–231Google Scholar
  60. Paltto H, Nordberg A, Nordén B, Snäll T (2011) Development of secondary woodland in oak wood pastures reduces the richness of rare epiphytic lichens. PLoSOne 6:e24675Google Scholar
  61. Pautasso M, Aas G, Queloz V, Holdenrieder O (2013) European ash (Fraxinus excelsior) dieback—a conservation biology challenge. Biol Cons 158:37–49Google Scholar
  62. Pearce J, Ferrier S (2000) Evaluating the predictive performance of habitat models developed using logistic regression. Ecol Model 133:225–245Google Scholar
  63. Penoyre J (2005) Traditional Houses of Somerset. Somerset Books, TivertonGoogle Scholar
  64. Penoyre J, Penoyre J (1978) Houses in the landscape: a regional study of vernacular building styles in England and Wales. Faber, LondonGoogle Scholar
  65. Perry M, Hollis D (2005) The generation of monthly gridded datasets for a range of climatic variables over the UK. Int J Climatol 25:1041–1054Google Scholar
  66. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259Google Scholar
  67. Rackham O (1972) Grundle House: on the quantities of timber in certain East Anglian buildings in relation to local supplies. Vernac Archit 3:3–8Google Scholar
  68. Rackham O (1986) The history of the countryside. Phoenix Press, LondonGoogle Scholar
  69. Rackham O (2006) Woodlands. Collins, LondonGoogle Scholar
  70. Rackham O (2008) Ancient woodland: modern threats. New Phytol 180:571–586PubMedGoogle Scholar
  71. Rands MRW, Adams WM, Bennun L, Butchart SHM, Clements A, Coomes D, Entwistle A, Hodge I, Kapos V, Scharlemann JPW, Sutherland WJ, Vira B (2010) Biodiversity conservation: challenges beyond 2010. Science 329:1298–1303PubMedGoogle Scholar
  72. Raustiala K, Victor DG (1996) Biodiversity since rio: the future of the convention of biological diversity. Environment 38:1–11Google Scholar
  73. Roberts AJ, Russel C, Walker GJ, Kirby KJ (1992) Regional variation in the origin, extent and composition of Scottish woodland. Bot J Scotl 46:167–189Google Scholar
  74. Rodwell JS (1991) British Plant Communities volume 1 Woodlands and Scrub. Cambridge University Press, CambridgeGoogle Scholar
  75. Rose F (1974) The epiphytes of oak. In: Morris MG, Perring FH (eds) The british oak. EW Classey, London, pp 250–273Google Scholar
  76. Rose F (1976) Lichenological indicators of age and environmental continuity in woodlands. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic Press, London and New York, pp 279–307Google Scholar
  77. RoTAP (2012) Review of transboundary air pollution: acidification, eutrophication, ground level ozone and heavy metals in the UK. CEH, EdinburghGoogle Scholar
  78. Sachs J, Reid WV (2006) Investments towards sustainable development. Science 312:1002PubMedGoogle Scholar
  79. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity senarios for the year 2100. Science 287:1770–1774PubMedGoogle Scholar
  80. Seaward MRD (1998) Time-space analysis of the British lichen flora, with particular reference to air quality surveys. Folia Cryptogamica Estonica 32:85–96Google Scholar
  81. Selva SB (1994) Lichen diversity and stand continuity in the northern hardwoods and spruce-fir forests of northern New England and western New Brunswick. The Bryol 97:424–429Google Scholar
  82. Shafer CL (1999) history of selection and system planning for US natural area national parks and monuments: beauty and biology. Biodivers Conserv 8:189–204Google Scholar
  83. Sillett SC, McCune B, Peck JE, Rambo TR, Ruchty A (2000) Dispersal limitations of epiphytic lichens result in species dependent on old-growth forests. Ecol Appl 10:789–799Google Scholar
  84. Slocombe P (1997) Re-used carpentry showing evidence of earlier or archaic carpentry. Vernac Archit 28:122–123Google Scholar
  85. Smith PL (2014) Lichen translocation with reference to species conservation and habitat restoration. Symbiosis 62:17–28Google Scholar
  86. Spencer JW, Kirby KJ (1992) An inventory of ancient woodland for England and Wales. Biol Cons 62:77–93Google Scholar
  87. Swetnam TW, Allen CD, Betancourt JL (1999) Applied historical ecology: using the past to manage for the future. Ecol Appl 9:1189–1206Google Scholar
  88. Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293PubMedGoogle Scholar
  89. Tabor K, Burgess ND, Mbilinyi BP, Kashaigili JJ, Steininger MK (2010) Forest and woodland cover and change in coastal Tanzania and Kenya, 1990 to 2000. J East Afr Nat Hist 99:19–45Google Scholar
  90. Tedersoo L, Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytol 185:351–354PubMedGoogle Scholar
  91. Tedersoo L, Bahram M, Toots M, Diédhiou AG, Henkel TW, Kjøller R, Morris MH, Nara K, Nouhra E, Peay KG, Põlme S, Ryberg M, Smith ME, Kõljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21:4160–4170PubMedGoogle Scholar
  92. Tibell L (1992) Crustose lichens as indicators of forest continuity in boreal coniferous forests. Nord J Bot 12:427–450Google Scholar
  93. Tyson B (1987) Building accounts for enlarging a farm building at Maulds Meaburn Cumbria. Vernac Archit 18:17–24Google Scholar
  94. Tyson B (1998) Transportation and the supply of construction materials: an aspect of traditional building management. Vernac Archit 29:63–81Google Scholar
  95. Van Herk CM, Mathijssen-Spiekman EAM, De Zwart D (2003) Long distance nitrogen air pollution effects on lichens in Europe. The Lichenol 35:347–359Google Scholar
  96. Varlow P (2015) From trees to timbers: a compartive study of timber quantities in houses. Vernac Archit 46:66–81Google Scholar
  97. Vedeld P, Jumane A, Wapalila G, Songorwa AN (2012) Protected areas, poverty and conflicts: a livelihood case study of Mikumi National Park, Tanzania. For Pol Econ 21:20–31Google Scholar
  98. 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 7:3663–3681Google Scholar
  99. Watson MF, Hawksworth DL, Rose F (1988) Lichens on elms in the British Isles and the effect of Dutch elm disease on their status. The Lichenol 20:327–352Google Scholar
  100. Whittet R, Ellis CJ (2013) Critical tests for lichen indicators of woodland ecological continuity. Biol Cons 168:19–23Google Scholar
  101. Wild R, Moir A (2013) Key dating features for timber-framed dwellings in Surrey. Vernac Archit 44:46–61Google Scholar
  102. Wolseley PA, James PW, Theobald MR, Sutton MA (2006) Detecting changes in epiphytic lichen communities at sites affected by atmospheric ammonia from agricultural sources. Lichenologist 38:161–176Google Scholar
  103. Woodbridge J, Fyfe RM, Roberts N, Downey S, Edinborough K, Shennan S (2014) The impact of Neolithic transition in Britain: a comparison of pollen-based land-cover and archaeological 14C date-inferred population change. J Archaeol Sci 51:216–224Google Scholar
  104. Woodin SJ (1989) Environmental effects of air pollution in Britain. J Appl Ecol 26:749–761Google Scholar
  105. Yahr R, Ellis CJ (2009) Lichens in the attic. Build Conserv Direct 2009:13–14Google Scholar
  106. Yahr R, Coppins BJ, Ellis CJ (2011) Preserved epiphytes as an archaeological resource in pre-industrial vernacular buildings. J Archaeol Sci 38:1191–1198Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Royal Botanic Garden EdinburghEdinburghUK

Personalised recommendations