Specialist species of wood‐inhabiting fungi struggle while generalists thrive in fragmented boreal forests

Summary The loss of suitable habitats is one of the main causes behind the loss of species and communities. Habitat fragmentation, that is, the division of the remaining habitat into small and isolated fragments, often co-occurs with the process of habitat loss. The spatial division of habitats decreases connectivity among local populations and generally has a negative effect on population viability, but it can also have a positive effect for some species, for example, due to released competition pressure. In both animals and plants, certain characteristics such as low dispersal ability and narrow ecological niche are known to be associated with fragmentation vulnerability, but in fungi, systematic analyses have so far been lacking. With their small and highly dispersive spores, fungi could be mainly resource-limited, not dispersal-limited. In this study, we analysed spatial occurrence data on 119 species of wood-inhabiting fungi to identify the species characteristics that are associated with high extinction risk and fragmentation vulnerability in particular. We modelled resource use and connectivity dependence separately for each species using the presence–absence data on 98 318 dead trees in 496 sites located on a gradient in the duration and intensity of land use in eastern Fennoscandia. We then related species' responses to connectivity to their resource-use patterns, life-history characteristics and red-list status. Our results show that red-listed species are highly specialized in their resource use and suffer from loss of connectivity at three spatial scales: along the large-scale gradient, at the landscape scale and at the scale of a forest stand. In contrast, many of the non-red-listed generalist species are actually more likely to occur (per resource unit) in fragmented managed forests than well-connected natural forests. Synthesis. We show that the expected number of red-listed species per a fixed amount of similar resources (dead trees) can be even more than 10 times higher in well-connected than in fragmented surroundings, and thus, protecting high-quality areas that are well connected is conservationally more effective than protecting small fragments distributed across the landscape.

[1]  Assessing the extinction vulnerability of wood-inhabiting fungal species in fragmented northern Swedish boreal forests , 2008 .

[2]  J. Siitonen,et al.  Significance of woodland key habitats for polypore diversity and red-listed species in boreal forests , 2008, Biodiversity and Conservation.

[3]  J. Siitonen,et al.  Coarse woody debris, polyporous fungi and saproxylic insects in an old-growth spruce forest in Vodlozero National Park, Russian Karelia , 2001 .

[4]  D. Lindenmayer,et al.  Ecological continuity and assumed indicator fungi in boreal forest: the importance of the landscape matrix , 2003 .

[5]  Teja Tscharntke,et al.  Characteristics of insect populations on habitat fragments: A mini review , 2002, Ecological Research.

[6]  P. Martikainen,et al.  Methane fluxes on boreal peatlands of different fertility and the effect of long‐term experimental lowering of the water table on flux rates , 1998 .

[7]  J. Stenlid,et al.  Selective replacement between species of wood-rotting basidiomycetes, a laboratory study , 1997 .

[8]  Tiina Markkanen,et al.  Modeling air-mediated dispersal of spores, pollen and seeds in forested areas , 2007 .

[9]  T. Székely,et al.  Can intrinsic factors explain population declines in North American breeding shorebirds? A comparative analysis , 2006 .

[10]  L. Boddy,et al.  Chapter 14 Distribution patterns of wood-decay basidiomycetes at the landscape to global scale , 2008 .

[11]  T. Snäll,et al.  Edge effects on six polyporous fungi used as old-growth indicators in Swedish boreal forest , 2001 .

[12]  A. Komonen,et al.  Conservation ecology of boreal polypores: A review , 2011 .

[13]  Kevin McGarigal,et al.  COMPARATIVE EVALUATION OF EXPERIMENTAL APPROACHES TO THE STUDY OF HABITAT FRAGMENTATION EFFECTS , 2002 .

[14]  L. Ryvarden,et al.  Relationship between basidiospore size, shape and life history characteristics: a comparison of polypores , 2008 .

[15]  J. Heilmann‐Clausen,et al.  Diversity of dead wood inhabiting fungi and bryophytes in semi-natural beech forests in Europe , 2006 .

[16]  T. Kuuluvainen,et al.  Structure of old Pinus sylvestris dominated forest stands along a geographic and human impact gradient in mid-boreal Fennoscandia , 2005 .

[17]  I. Hanski The shrinking world : ecological consequences of habitat loss , 2005 .

[18]  N. Tuno Insect feeding on spores of a bracket fungus, Elfvingia applanata (Pers.) Karst. (Ganodermataceae, Aphyllophorales) , 1999, Ecological Research.

[19]  C. Margules,et al.  Predictors of Species Sensitivity to Fragmentation , 2004, Biodiversity & Conservation.

[20]  T. Snäll,et al.  Mating system, reproduction mode and diaspore size affect metacommunity diversity , 2009 .

[21]  Lenore Fahrig,et al.  INDEPENDENT EFFECTS OF FOREST COVER AND FRAGMENTATION ON THE DISTRIBUTION OF FOREST BREEDING BIRDS , 1999 .

[22]  Juha Siitonen,et al.  Forest management, coarse woody debris and saproxylic organisms: Fennoscandian boreal forests as an example , 2001 .

[23]  T. Kuuluvainen,et al.  Coarse woody debris in old Pinus sylvestris dominated forests along a geographic and human impact gradient in boreal Fennoscandia , 2002 .

[24]  K. Høiland,et al.  Biodiversity of wood‐inhabiting fungi in a boreal coniferous forest in Ser‐Trendelag County, Central Norway , 1996 .

[25]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[26]  J. Heilmann‐Clausen,et al.  Wood-inhabiting macrofungi in Danish beech-forests – conflicting diversity patterns and their implications in a conservation perspective , 2005 .

[27]  J. L. Gittleman,et al.  Predicting extinction risk in declining species , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  Otso Ovaskainen,et al.  A unified measure of the number, volume and diversity of dead trees and the response of fungal communities , 2009 .

[29]  J. Stenlid,et al.  Abundance and viability of fungal spores along a forestry gradient – responses to habitat loss and isolation? , 2004 .

[30]  K. Larsson,et al.  Legacies from natural forest dynamics: Different effects of forest management on wood-inhabiting fungi in pine and spruce forests , 2011 .

[31]  O. Honnay,et al.  The relative importance of local, regional and historical factors determining the distribution of plants in fragmented riverine forests: an emergent group approach , 2005 .

[32]  B. Jonsson,et al.  Spore deposition of wood-decaying fungi: importance of landscape composition , 2004 .

[33]  Lars Östlund,et al.  The history and transformation of a Scandinavian boreal forest landscape since the 19th century , 1997 .

[34]  J. Kouki,et al.  Are woodland key habitats in Finland hotspots for polypores (Basidiomycota)? , 2006 .

[35]  Martin-Hugues St-Laurent,et al.  Dissecting habitat loss and fragmentation effects following logging in boreal forest: Conservation perspectives from landscape simulations , 2009 .

[36]  J. Siitonen,et al.  Polypore diversity in managed and old-growth boreal Picea abies forests in southern Finland , 2004 .

[37]  M. Aizen,et al.  Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. , 2006, Ecology letters.

[38]  R. Didham,et al.  Confounding factors in the detection of species responses to habitat fragmentation , 2005, Biological reviews of the Cambridge Philosophical Society.

[39]  T. Ahti,et al.  Vegetation zones and their sections in northwestern Europe , 1968 .

[40]  L. Barbaro,et al.  Linking bird, carabid beetle and butterfly life-history traits to habitat fragmentation in mosaic landscapes , 2009 .

[41]  R. O’Hara,et al.  Quantifying Habitat Requirements of Tree‐Living Species in Fragmented Boreal Forests with Bayesian Methods , 2009, Conservation biology : the journal of the Society for Conservation Biology.

[42]  J. Siitonen,et al.  Linking substrate and habitat requirements of wood-inhabiting fungi to their regional extinction vulnerability , 2011 .

[43]  T. Spanhove,et al.  Forest fragmentation relaxes natural nest predation in an Afromontane forest , 2009 .

[44]  Walter Krämer,et al.  Review of Modern applied statistics with S, 4th ed. by W.N. Venables and B.D. Ripley. Springer-Verlag 2002 , 2003 .

[45]  O. Ovaskainen,et al.  Extinction Debt at Extinction Threshold , 2002 .

[46]  Kate E. Jones,et al.  The predictability of extinction: biological and external correlates of decline in mammals , 2008, Proceedings of the Royal Society B: Biological Sciences.

[47]  M. Siitonen,et al.  Effects of Forest Edges on the Distribution, Abundance, and Regional Persistence of Wood‐Rotting Fungi , 2005 .

[48]  P. Martikainen,et al.  Fallen retention aspen trees on clear-cuts can be important habitats for red-listed polypores: a case study in Finland , 2007, Biodiversity and Conservation.

[49]  J. Müller,et al.  Effects of resource availability and climate on the diversity of wood‐decaying fungi , 2010 .

[50]  T. O. Crist,et al.  Habitat specialization, body size, and family identity explain lepidopteran density–area relationships in a cross-continental comparison , 2007, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Susanne A. Fritz,et al.  Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. , 2009, Ecology letters.

[52]  F. Anselmet,et al.  Aerosol dry deposition on vegetative canopies. Part I: Review of present knowledge , 2008 .

[53]  I. Hanski,et al.  Consequences of forest fragmentation for polyporous fungi at two spatial scales , 2006 .

[54]  R. Holt,et al.  A Survey and Overview of Habitat Fragmentation Experiments , 2000 .

[55]  Robert A. Davis,et al.  Habitat Fragmentation and Landscape Change: An Ecological and Conservation Synthesis , 2006 .

[56]  Peter Kareiva,et al.  Habitat Destruction, Fragmentation, and Disturbance Promote Invasion by Habitat Generalists in a Multispecies Metapopulation , 2004, Risk analysis : an official publication of the Society for Risk Analysis.

[57]  M. Dorcas,et al.  Habitat specificity and home‐range size as attributes of species vulnerability to extinction: a case study using sympatric rattlesnakes , 2006 .

[58]  J. Gower A General Coefficient of Similarity and Some of Its Properties , 1971 .

[59]  T. Mitakakis,et al.  The effect of sunlight on allergen release from spores of the fungus Alternaria , 2003 .

[60]  B. Jonsson,et al.  Predictability of plant and fungal species richness of old‐growth boreal forest islands , 2001 .

[61]  G. Várkonyi,et al.  Effects of habitat quality and landscape structure on saproxylic species dwelling in boreal spruce-swamp forests , 2008 .