At least 10% of the world’s tree species are threatened with extinction and pathogens are increasingly implicated in tree threats. Coextinction and threats to affiliates as a consequence of the loss or decline of their host trees is a poorly understood phenomenon. Ash dieback is an emerging infectious disease causing severe dieback of common ash Fraxinus excelsior throughout Europe. We utilized available empirical data on affiliate epiphytic lichen diversity (174 species and 17,800 observations) among 20 ash dieback infected host tree populations of F. excelsior on the island Gotland in the Baltic Sea, Sweden. From this, we used structured scenario projections scaled with empirical data of ash dieback disease to generate probabilistic models for estimating local and regional lichen coextinction risks. Average coextinction probabilities (ā) were 0.38 (95% CI ±0.09) for lichens occurring on F. excelsior and 0.14 (95% CI ±0.03) when considering lichen persistence on all tree species. ā was strongly linked to local disease incidence levels and generally increasing with lichen host specificity to F. excelsior and decreasing population size. Coextinctions reduced affiliate community viability, with significant local reductions in species richness and shifts in lichen species composition. Affiliates were projected to become locally extirpated before their hosts, illuminating the need to also consider host tree declines. Traditionally managed open wooded meadows had the highest incidence of ash dieback disease and significantly higher proportions of affiliate species projected to go extinct, compared with unmanaged closed forests and semi-open grazed sites. Most cothreatened species were not previously red-listed, which suggest that tree epidemics cause many unforeseen threats to species. Our analysis shows that epidemic tree deaths represent an insidious, mostly overlooked, threat to sessile affiliate communities in forested environments. Current conservation and management strategies must account for secondary extinctions associated with epidemic tree death.
References
[1]
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287: 443–449.
[2]
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, et al. (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296: 2158–2162.
[3]
Smith KF, Dobson AP, McKenzie FE, Real LA, Smith DL, et al. (2005) Ecological theory to enhance infectious disease control and public health policy. Front Ecol Environ 3: 29–37.
[4]
Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20: 1349–1357.
[5]
La Porta N, Capretti P, Thomsen IM, Kasanen R, Hietala AM, et al. (2008) Forest pathogens with higher damage potential due to climate change in Europe. Can J Plant Pathol 30: 177–195.
[6]
Loo JA (2009) Ecological impacts of non–indigenous invasive fungi as forest pathogens. Biol Invasions 11: 81–96.
[7]
Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, et al. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484: 186–194.
[8]
Kowalski T, Holdenrieder O (2009) The teleomorph of Chalara fraxinea, the causal agent of ash dieback. Forest Pathol 39: 304–308.
[9]
Juodvalkis A, Vasiliauskas A (2002) The extent and possible causes of dieback of ash stands in Lithuania. LZUU Mokslo Darbai, Biomedicinos Mokslai 56: 17–22 (in Lithuanian with English summary)..
[10]
Kowalski T (2006) Chalara fraxinea sp. nov. associated with dieback of ash (Fraxinus excelsior) in Poland. Forest Pathol 36: 264–270.
[11]
Bakys R, Vasaitis R, Barklund P, Ihrmark K, Stenlid J (2009) Investigations concerning the role of Chalara fraxinea in declining Fraxinus excelsior. Plant Pathol 58: 284–292.
[12]
Bakys R, Vasaitis R, Barklund P, Thomsen IM, Stenlid J (2009) Occurrence and pathogenicity of fungi in necrotic and non–symptomatic shoots of declining common ash (Fraxinus excelsior) in Sweden. Eur J Forest Res 128: 51–60.
[13]
Castello JD, Leopold DJ, Smallidge PJ (1995) Pathogens, patterns, and processes in forest ecosystems. BioScience 45: 16–24.
[14]
Ellison AM, et al. (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3: 479–486.
[15]
Lindenmayer DB, Likens GE, Franklin JF (2010) Rapid responses to facilitate ecological discoveries from major disturbances. Front Ecol Environ 8: 527–532.
[16]
Ebenman B, Law R, Borrvall C (2004) Community viability analysis, the response of ecological communities to species loss. Ecology 85: 2591–2600.
[17]
Ebenman B, Jonsson T (2005) Using community viability analysis to identify fragile systems and keystone species. Trends Ecol Evol 20: 568–575.
[18]
Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, et al. (2004) Species coextinctions and the biodiversity crisis. Science 305: 1632–1634.
[19]
Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? P Roy Soc B 276: 3037–2045.
[20]
Moir ML, Vesk PA, Brennan KEC, Keith DA, Hughes L, et al. (2010) Current constraints and future directions in estimating coextinction. Conserv Biol 24: 682–690.
[21]
G?rdenfors U (2010) The 2010 Red List of Swedish Species. ArtDatabanken, SLU, Uppsala.
[22]
McKinney LV, Nielsen LR, Hansen JK, Kj?r ED (2011) Presence of natural genetic resistance in Fraxinus excelsior (Oleraceae) to Chalara fraxinea (Ascomycota): an emerging infectious disease. Heredity 106: 788–797.
[23]
Thor G, Johansson P, J?nsson MT (2010) Lichen diversity and red–listed lichen species relationships with tree species and diameter in wooded meadows. Biodiv Conserv 19: 2307–2328.
[24]
Santesson R, Moberg R, Nordin A, T?nsberg T, Vitikainen O (2004) Lichen–forming and lichenicolous fungi of Fennoscandia. Museum of Evolution, Uppsala University, Sweden.
[25]
Krok TH, Almquist S (2001) Svensk flora, fanerogamer och ormbunksv?xter. 28 edn. Liber f?rlag, Stockholm (In Swedish).
[26]
Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, et al.. (2009) The Lichens of Great Britain and Ireland. London: The British Lichen Society.
[27]
Eskelson BNI, Madsen L, Hagar JC, Temesgen H (2011) Estimating Riparian Understory Vegetation Cover with Beta Regression and Copula Models. Forest Sci 57: 212–221.
[28]
Cribari-Neto F, Zeileis A (2010) Beta Regression in R. J Stat Softw. 34: 1–24.
[29]
Gelman A, Hill J (2007) Data Analysis Using Regression and Multilevel/Hierarchical Models. Cambridge, New York.
[30]
Clarke KR (1993) Non–parametric multivariate analysis of changes in community structure. Aust J Ecol 18: 117–143.
[31]
Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero–adjusted Bray–Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330: 55–80.
[32]
Hammer ?, Harper DAT, Ryan PD (2001) PAST, paleontological statistics soft–ware package for education and data analysis. Palaeontol Electron 4: 1–9.
[33]
Taguchi Y, Oono Y (2005) Relational patterns of gene expression via non–metric multidimensional scaling analysis. Bioinformatics 21: 730–740.
[34]
Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a non–metric hypothesis. Psychometrika 29: 1–27.
[35]
Pli?ra A, Lygis V, Suchockas V, Bartkevi?ius E (2011) Performance of twenty four European Fraxinus excelsior populations in three Lithuanian progeny trials with a special emphasis on resistance to Chalara fraxinea. Baltic Forestry 17: 17–34.
[36]
Tilman D (2001) Functional diversity. Pages 109–120 in Levin, S.A., editor. Encyclopedia of Biodiversity. Academic Press, San Diego, CA.
[37]
P?ykk? H, Hyv?rinen M (2003) Host preference and performance of lichenivorous Eilema spp. larvae in relation to lichen secondary metabolites. J Anim Ecol 72: 383–390.
[38]
Asplund J, Larsson P, Vatne S, Gauslaa Y (2010) Gastropod grazing shapes the vertical distribution of epiphytic lichens in forest canopies. J Ecol 98: 218–225.
[39]
Sn?ll T, Riberio Jr J, Rydin H (2003) Spatial occurrence and colonizations in patch–tracking metapopulations: local conditions versus dispersal. Oikos 103: 566–578.
[40]
Rose F, Wolseley P (1984) Nettlecombe Park – its history and its epiphytic lichens, an attempt at correlation. Field Studies 6: 117–148.
[41]
Roberge J–M, Bengtsson SBK, Wulff S, Sn?ll T (2011) Edge creation and tree dieback influence the patch–tracking metapopulation dynamics of a red–listed epiphytic bryophyte. J Appl Ecol 48: 650–658.
[42]
Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographic space. Trends Parasitol 27: 355–361.
[43]
L?hmus P (2003) Composition and substrata of forest lichens in Estonia: a meta–analysis. Folia Cryptogamica Estonica 40: 19–38.
[44]
Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, et al. (2002) Biodiversity as a barrier to ecological invasion. Nature 417: 636–638.
[45]
Jones JT, Moens M, Mota M, Li H, Kikuchi T (2008) Bursaphelenchus xylophilus, opportunities in comparative genomics and molecular host–parasite interactions. Mol Plant Pathol 9: 357–368.
[46]
Oldfield SF, Lusty C, Mackinven A (1998) The world list of threatened trees. World Conservation Press, Cambridge, UK.