Skip to main content

Advertisement

Log in

The ‘chicken or the egg’: which comes first, forest tree decline or loss of mycorrhizae?

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Forest trees are experiencing massive declines globally caused by a multitude of stressors, both abiotic (pollution, fragmentation and climate change) and biotic (fungi, bacteria, viruses and insects). Mycorrhizal fungi aid plants in the requisition of nutrients through their mutualistic relationship with plant roots and are integral to tree health. Stresses affecting tree health will also influence mycorrhizal fungi directly or indirectly, and thus alter the pathways responsible for nutrient absorption. Such an intimate association is a true chicken or egg quandary; do external stressors cause a loss of mycorrhizae which leads to tree decline, does tree decline result in a loss of mycorrhizae, or is it a combination of both? A review of literature has identified six stressors known to contribute to tree decline and to impact directly on mycorrhizae; global climate change, pesticides, heavy metals, excess fertilizer, pathogens and habitat fragmentation. A few review papers have highlighted the link; however, what is missing is irrefutable empirical research. This review documents the known direct impacts of the six stressors on mycorrhizal communities and places this in the context of decline syndromes in long-lived forest trees. We also discuss methodologies available to identify fungi and future research needed to unravel the complex relationships between forest tree declines and their associated mycorrhizal fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169:704–709. doi:10.1016/j.jplph.2012.01.014

    Article  CAS  PubMed  Google Scholar 

  • Acácio V, Dias FS, Catry FX, Rocha M, Moreira F (2016) Landscape dynamics in Mediterranean oak forests under global change: understanding the role of anthropogenic and environmental drivers across forest types. Glob Change Biol 23:1199–1217. doi:10.1111/gcb.13487

    Article  Google Scholar 

  • Albornoz FE, Burgess TI, Lambers H, Etchells H, Laliberté E (2016) Native soilborne pathogens equalize differences in competitive ability between plants of contrasting nutrient-acquisition strategies. J Ecol 105:549–557. doi:10.1111/1365-2745.12638

    Article  Google Scholar 

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684. doi:10.1016/j.foreco.2009.09.001

    Article  Google Scholar 

  • Anderson P, Brundrett M, Grierson P, Robinson R (2010) Impact of severe forest dieback caused by Phytophthora cinnamomi on macrofungal diversity in the northern jarrah forest of Western Australia. For Ecol Manage 259:1033–1040. doi:10.1016/j.foreco.2009.12.015

    Article  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701

    Article  CAS  PubMed  Google Scholar 

  • Barber PA, Paap T, Burgess TI, Dunstan W, Hardy GESJ (2013) A diverse range of Phytophthora species are associated with dying urban trees. Urban For Urban Green 12:569–575. doi:10.1016/j.ufug.2013.07.009

    Article  Google Scholar 

  • Bellgard SE, Williams SE (2011) Response of mycorrhizal diversity to current climatic changes. Diversity 3:8–90. doi:10.3390/d3010008

    Article  CAS  Google Scholar 

  • Bignal KL, Ashmore MR, Headley AD (2008) Effects of air pollution from road transport on growth and physiology of six transplanted bryophyte species. Environ Pollut 156:332–340. doi:10.1016/j.envpol.2008.02.011

    Article  CAS  PubMed  Google Scholar 

  • Blom J, Vannini A, Vettraino A, Hale M, Godbold D (2009) Ectomycorrhizal community structure in a healthy and a Phytophthora-infected chestnut (Castanea sativa Mill.) stand in central Italy. Mycorrhiza 20:25–38. doi:10.1007/s00572-009-0256-z

    Article  PubMed  Google Scholar 

  • Blood A, Starr G, Escobedo F, Chappelka A, Staudhammer C (2016) How do urban forests compare? Tree diversity in urban and periurban forests of the southeastern US. Forests 7:120

    Article  Google Scholar 

  • Branzanti BM, Rocca E, Pisi A (1999) Effect of ectomycorrhizal fungi on chestnut ink disease. Mycorrhiza 9:103–109. doi:10.1007/s005720050007

    Article  Google Scholar 

  • Brasier CM (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol 57:792–808

    Article  Google Scholar 

  • Braun S, Thomas VFD, Quiring R, Flückiger W (2010) Does nitrogen deposition increase forest production? The role of phosphorus. Environ Pollut 158:2043–2052. doi:10.1016/j.envpol.2009.11.030

    Article  CAS  PubMed  Google Scholar 

  • Breckle S-W, Kahle H (1992) Effects of toxic heavy metals (Cd, Pb) on growth and mineral nutrition of beech (Fagus sylvatica L.). Vegetatio 101:43–53. doi:10.1007/bf00031914

    Article  Google Scholar 

  • Brouwers N, Matusick G, Ruthrof K, Lyons T, Hardy G (2013) Landscape-scale assessment of tree crown dieback following extreme drought and heat in a Mediterranean eucalypt forest ecosystem. Landsc Ecol 28:69–80

    Article  Google Scholar 

  • Brundrett M (1991) Mycorrhizas in natural ecosystems. In: Begon M, Fitter AH, Macfadyen A (eds) Advances in ecological research, vol 21. Academic Press, Cambridge, pp 171–313. doi:10.1016/S0065-2504(08)60099-9

    Chapter  Google Scholar 

  • Brundrett MC, Abbott LK (1995) Mycorrhizal fungus propagules in the jarrah forest. II. Spatial variability in inoculum levels. New Phytol 131:461–469. doi:10.2307/2558916

    Article  Google Scholar 

  • Brundrett M, Bougher N, Dell B, Grove T (1996) Working with mycorrhizas in forestry and agriculture. ACIAR monograph. ACIAR, Canberra

    Google Scholar 

  • Burgess TI, Malajczuk N, Grove TS (1993) The ability of 16 ectomycorrhizal fungi to increase growth and phosphorus uptake of Eucalyptus globulus Labill. and E. diversicolor F. Muell. Plant Soil 153:155–164

    Article  CAS  Google Scholar 

  • Burgess TI, Scott JK, McDougall KL, Stukely MJC, Crane C, Dunstan WA, Brigg F, Andjic V, White D, Rudman T, Arentz F, Ota N, Hardy GESJ (2016) Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Glob Change Biol. doi:10.1111/gcb.13492

    Google Scholar 

  • Cahill JF, Cale JA, Karst J, Bao T, Pec GJ, Erbilgin N (2016) No silver bullet: different soil handling techniques are useful for different research questions, exhibit differential type I and II error rates, and are sensitive to sampling intensity. New Phytol. doi:10.1111/nph.14141

    Google Scholar 

  • Cairney JWG (2011) Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils. Plant Soil 344:51–71. doi:10.1007/s11104-011-0731-0

    Article  CAS  Google Scholar 

  • Cekstere G, Osvalde A (2013) A study of chemical characteristics of soil in relation to street trees status in Riga (Latvia). Urban For Urban Green 12:69–78. doi:10.1016/j.ufug.2012.09.004

    Article  Google Scholar 

  • Cobb RC, Meentemeyer RK, Rizzo DM (2016) Wildfire and forest disease interaction lead to greater loss of soil nutrients and carbon. Oecologia. doi:10.1007/s00442-016-3649-7

    PubMed  Google Scholar 

  • Corcobado T, Vivas M, Moreno G, Solla A (2014) Ectomycorrhizal symbiosis in declining and non-declining Quercus ilex trees infected with or free of Phytophthora cinnamomi. For Ecol Manage 324:72–80. doi:10.1016/j.foreco.2014.03.040

    Article  Google Scholar 

  • Crockatt ME (2012) Are there edge effects on forest fungi and if so do they matter? Fungal Biol Rev 26:94–101. doi:10.1016/j.fbr.2012.08.002

    Article  Google Scholar 

  • Das AJ, Stephenson NL, Davis KP (2016) Why do trees die? Characterizing the drivers of background tree mortality. Ecology 97:2616–2627. doi:10.1002/ecy.1497

    Article  PubMed  Google Scholar 

  • Delavaux CS, Camenzind T, Homeier J, Jiménez-Paz R, Ashton M, Queenborough SA (2016) Nutrient enrichment effects on mycorrhizal fungi in an Andean tropical montane Forest. Mycorrhiza. doi:10.1007/s00572-016-0749-5

    PubMed  Google Scholar 

  • Deng Q, McMahon DE, Xiang Y, Yu C-L, Jackson RB, Hui D (2016) A global meta-analysis of soil phosphorus dynamics after afforestation. New Phytol 213:181–192. doi:10.1111/nph.14119

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Diaz R, Loague K (2001) Assessing the potential for pesticide leaching for the pine forest areas of Tenerife. Environ Toxicol Chem 20:1958–1967. doi:10.1002/etc.5620200914

    Article  CAS  PubMed  Google Scholar 

  • Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255. doi:10.1111/j.1365-2745.2005.00977.x

    Article  Google Scholar 

  • Druille M, García-Parisi PA, Golluscio RA, Cavagnaro FP, Omacini M (2016) Repeated annual glyphosate applications may impair beneficial soil microorganisms in temperate grassland. Agric Ecosyst Environ 230:184–190. doi:10.1016/j.agee.2016.06.011

    Article  CAS  Google Scholar 

  • Egli S (2011) Mycorrhizal mushroom diversity and productivity—an indicator of forest health? Ann For Sci 68:81–88. doi:10.1007/s13595-010-0009-3

    Article  Google Scholar 

  • Entry JA, Rygiewicz PT, Watrud LS, Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Adv Environ Res 7:123–138. doi:10.1016/S1093-0191(01)00109-5

    Article  CAS  Google Scholar 

  • Eschen R, Britton K, Brockerhoff E, Burgess T, Dalley V, Epanchin-Niell RS, Gupta K, Hardy G, Huang Y, Kenis M, Kimani E, Li HM, Olsen S, Ormrod R, Otieno W, Sadof C, Tadeu E, Theyse M (2015) International variation in phytosanitary legislation and regulations governing importation of plants for planting. Environ Sci Policy 51:228–237. doi:10.1016/j.envsci.2015.04.021

    Article  Google Scholar 

  • Fernandez CW, Koide RT (2013) The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecol 6:479–486. doi:10.1016/j.funeco.2013.08.004

    Article  Google Scholar 

  • Fernandez CW, Nguyen NH, Stefanski A, Han Y, Hobbie SE, Montgomery RA, Reich PB, Kennedy PG (2016) Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal-temperate ecotone. Glob Change Biol 23:1598–1609. doi:10.1111/gcb.13510

    Article  Google Scholar 

  • Fleming PA, Anderson H, Prendergast AS, Bretz MR, Valentine LE, Hardy GES (2014) Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function? Mamm Rev 44:94–108. doi:10.1111/mam.12014

    Article  Google Scholar 

  • Fransson P (2012) Elevated CO2 impacts ectomycorrhiza-mediated forest soil carbon flow: fungal biomass production, respiration and exudation. Fungal Ecol 5:85–98. doi:10.1016/j.funeco.2011.10.001

    Article  Google Scholar 

  • Frey SD, Ollinger S, Nadelhoffer K, Bowden R, Brzostek E, Burton A, Caldwell BA, Crow S, Goodale CL, Grandy AS, Finzi A, Kramer MG, Lajtha K, LeMoine J, Martin M, McDowell WH, Minocha R, Sadowsky JJ, Templer PH, Wickings K (2014) Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry 121:305–316. doi:10.1007/s10533-014-0004-0

    Article  CAS  Google Scholar 

  • Gonzalez P, Tucker CJ, Sy H (2012) Tree density and species decline in the African Sahel attributable to climate. J Arid Environ 78:55–64. doi:10.1016/j.jaridenv.2011.11.001

    Article  Google Scholar 

  • Halofsky J, Peterson D, Metlen K, Myer M, Sample V (2016) Developing and implementing climate change adaptation options in forest ecosystems: a case study in southwestern Oregon, USA. Forests 7:268

    Article  Google Scholar 

  • Hart MM, Aleklett K, Chagnon P-L, Egan C, Ghignone S, Helgason T, Lekberg Y, Öpik M, Pickles BJ, Waller L (2015) Navigating the labyrinth: a guide to sequence-based, community ecology of arbuscular mycorrhizal fungi. New Phytol 207:235–247. doi:10.1111/nph.13340

    Article  PubMed  Google Scholar 

  • Heng G, Hyde KD, Jianchu X, Valentine AJ, Mortimer PE (2016) Mycosphere essays 4. Mycorrhizal-associated nutrient dynamics in key ecosystems and their response to a changing environment. Mycosphere 7:190–203. doi:10.5943/mycosphere/7/2/8

    Google Scholar 

  • Henry C, Raivoarisoa J, Razafimamonjy A, Ramanankierana H, Andrianaivomahefa P, Ducousso M, Selosse M (2016) Characterization of ectomycorrhizal communities of Asteropeia mcphersonii seedlings spontaneously growing in natural forest and in open disturbed areas. Bot Lett 163:1–7. doi:10.1080/23818107.2016.1160327

    Google Scholar 

  • Hobbs RJ (2001) Synergisms among habitat fragmentation, livestock grazing, and biotic invasions in southwestern Australia. Conserv Biol 15:1522–1528. doi:10.1046/j.1523-1739.2001.01092.x

    Article  Google Scholar 

  • Huang J, Nara K, Zong K, Wang J, Xue S, Peng K, Shen Z, Lian C (2014) Ectomycorrhizal fungal communities associated with Masson pine (Pinus massoniana) and white oak (Quercus fabri) in a manganese mining region in Hunan Province, China. Fungal Ecol 9:1–10. doi:10.1016/j.funeco.2014.01.001

    Article  Google Scholar 

  • Hubbart JA, Guyette R, Muzika R-M (2016) More than drought: precipitation variance, excessive wetness, pathogens and the future of the western edge of the eastern deciduous forest. Sci Total Environ 566–567:463–467. doi:10.1016/j.scitotenv.2016.05.108

    Article  PubMed  CAS  Google Scholar 

  • Ihrmark K, Bödeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE, Lindahl BD (2012) New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677. doi:10.1111/j.1574-6941.2012.01437.x

    Article  CAS  PubMed  Google Scholar 

  • IPPC (2013) Climate change 2013: the physical science basis. IPCC and Cambridge University Press, Cambridge and New York

    Google Scholar 

  • Ipsilantis I, Samourelis C, Karpouzas DG (2012) The impact of biological pesticides on arbuscular mycorrhizal fungi. Soil Biol Biochem 45:147–155. doi:10.1016/j.soilbio.2011.08.007

    Article  CAS  Google Scholar 

  • Ishaq L, Barber P, Hardy GSJ, Calver M, Dell B (2013) Seedling mycorrhizal type and soil chemistry are related to canopy condition of Eucalyptus gomphocephala. Mycorrhiza 23:359–371. doi:10.1007/s00572-012-0476-5

    Article  CAS  PubMed  Google Scholar 

  • Jacobs FD, Timmer RV (2005) Fertilizer-induced changes in rhizosphere electrical conductivity: relation to forest tree seedling root system growth and function. New Forest 30:147–166. doi:10.1007/s11056-005-6572-z

    Article  Google Scholar 

  • Jönsson U (2004) Phytophthora species and oak decline—can a weak competitor cause significant root damage in a nonsterilized acidic forest soil? New Phytol 162:211–222. doi:10.1111/j.1469-8137.2004.01016.x

    Article  Google Scholar 

  • Jourand P, Ducousso M, Reid R, Majorel C, Richert C, Riss J, Lebrun M (2010) Nickel-tolerant ectomycorrhizal Pisolithus albus ultramafic ecotype isolated from nickel mines in New Caledonia strongly enhance growth of the host plant Eucalyptus globulus at toxic nickel concentrations. Tree Physiol 30:1311–1319. doi:10.1093/treephys/tpq070

    Article  CAS  PubMed  Google Scholar 

  • Karpouzas DG, Papadopoulou E, Ipsilantis I, Friedel I, Petric I, Udikovic-Kolic N, Djuric S, Kandeler E, Menkissoglu-Spiroudi U, Martin-Laurent F (2014) Effects of nicosulfuron on the abundance and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial toxicity. Ecol Indic 39:44–53. doi:10.1016/j.ecolind.2013.12.004

    Article  CAS  Google Scholar 

  • Keyser TL, Brown PM (2016) Drought response of upland oak (Quercus L.) species in Appalachian hardwood forests of the southeastern USA. Ann For Sci 73:1–16. doi:10.1007/s13595-016-0575-0

    Article  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CABI Publishing, Wallingford

    Google Scholar 

  • Kisko M, Bouain N, Rouached A, Choudhary SP, Rouached H (2015) Molecular mechanisms of phosphate and zinc signalling crosstalk in plants: phosphate and zinc loading into root xylem in Arabidopsis. Environ Exp Bot 114:57–64. doi:10.1016/j.envexpbot.2014.05.013

    Article  CAS  Google Scholar 

  • Laatikainen T, Heinonen-Tanski H (2002) Mycorrhizal growth in pure cultures in the presence of pesticides. Microbiol Res 157:127–137. doi:10.1078/0944-5013-00139

    Article  CAS  PubMed  Google Scholar 

  • Laurance WF, Ferreira LV, Rankin-de Merona JM, Laurance SG (1998) Rain forest fragmentation and the dynamics of amazonian tree communities. Ecology 79:2032–2040. doi:10.1890/0012-9658(1998)079[2032:RFFATD]2.0.CO;2

    Article  Google Scholar 

  • Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90. doi:10.1007/s00572-010-0348-9

    Article  PubMed  Google Scholar 

  • Leung H, Wang Z, Ye Z, Yung K, Peng X, Cheung K (2013) Interactions between arbuscular mycorrhizae and plants in phytoremediation of metal-contaminated soils: a review. Pedosphere 23:549–563. doi:10.1016/S1002-0160(13)60049-1

    Article  CAS  Google Scholar 

  • Liu L, Gundersen P, Zhang T, Mo J (2012a) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38. doi:10.1016/j.soilbio.2011.08.017

    Article  CAS  Google Scholar 

  • Liu Y, Shi G, Mao L, Cheng G, Jiang S, Ma X, An L, Du G, Collins Johnson N, Feng H (2012b) Direct and indirect influences of 8 year of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol 194:523–535. doi:10.1111/j.1469-8137.2012.04050.x

    Article  CAS  PubMed  Google Scholar 

  • Malajczuk N (1988) Interaction between Phytophthora cinnamomi zoospores and micro-organisms on non-mycorrhizal and ectomycorrhizal roots of Eucalyptus marginata. Trans Br Mycol Soc 90:375–382. doi:10.1016/S0007-1536(88)80146-3

    Article  Google Scholar 

  • Malmivaara-Lämsä M, Hamberg L, Haapamäki E, Liski J, Kotze DJ, Lehvävirta S, Fritze H (2008) Edge effects and trampling in boreal urban forest fragments—impacts on the soil microbial community. Soil Biol Biochem 40:1612–1621. doi:10.1016/j.soilbio.2008.01.013

    Article  CAS  Google Scholar 

  • Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: an overview with special reference to phytoremediation. Int J Environ Sci Technol 11:843–872. doi:10.1007/s13762-013-0299-8

    Article  CAS  Google Scholar 

  • Manion PD (1991) Tree disease concepts, 2nd edn. Prentice Hall Inc, New Jersey

    Google Scholar 

  • Matusick G, Ruthrof KX, Hardy GSJ (2012) Drought and heat triggers sudden and severe dieback in a dominant mediterranean-type woodland species. Open J For 2:183–186

    Google Scholar 

  • McCarren KL, McComb JA, Shearer BL, Hardy GESJ (2005) The role of chlamydospores of Phytophthora cinnamomi: a review. Australas Plant Pathol 34:333–338. doi:10.1071/ap05038

    Article  Google Scholar 

  • Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11:31–46. doi:10.1038/nrg2626

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto Y, Sakai A, Hattori M, Nara K (2015) Strong effect of climate on ectomycorrhizal fungal composition: evidence from range overlap between two mountains. ISME J 9:1870–1879. doi:10.1038/ismej.2015.8

    Article  PubMed  PubMed Central  Google Scholar 

  • Morrison EW, Frey SD, Sadowsky JJ, van Diepen LTA, Thomas WK, Pringle A (2016) Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest. Fungal Ecol 23:48–57. doi:10.1016/j.funeco.2016.05.011

    Article  Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. doi:10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  • Nilsson RH, Tedersoo L, Lindahl BD, Kjøller R, Carlsen T, Quince C, Abarenkov K, Pennanen T, Stenlid J, Bruns T, Larsson K-H, Kõljalg U, Kauserud H (2011) Towards standardization of the description and publication of next-generation sequencing datasets of fungal communities. New Phytol 191:314–318. doi:10.1111/j.1469-8137.2011.03755.x

    Article  Google Scholar 

  • Oßwald W, Fleischmann F, Rigling D, Coelho AC, Cravador A, Diez J, Dalio RJ, Horta Jung M, Pfanz H, Robin C, Sipos G, Solla A, Cech T, Chambery A, Diamandis S, Hansen E, Jung T, Orlikowski LB, Parke J, Prospero S, Werres S (2014) Strategies of attack and defence in woody plant–Phytophthora interactions. For Pathol 44:169–190. doi:10.1111/efp.12096

    Article  Google Scholar 

  • Perrier N, Amir H, Colin F (2006) Occurrence of mycorrhizal symbioses in the metal-rich lateritic soils of the Koniambo Massif, New Caledonia. Mycorrhiza 16:449–458. doi:10.1007/s00572-006-0057-6

    Article  PubMed  Google Scholar 

  • Peter M, Kohler A, Ohm RA, Kuo A, Krützmann J, Morin E, Arend M, Barry KW, Binder M, Choi C, Clum A, Copeland A, Grisel N, Haridas S, Kipfer T, LaButti K, Lindquist E, Lipzen A, Maire R, Meier B, Mihaltcheva S, Molinier V, Murat C, Pöggeler S, Quandt CA, Sperisen C, Tritt A, Tisserant E, Crous PW, Henrissat B, Nehls U, Egli S, Spatafora JW, Grigoriev IV, Martin FM (2016) Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nat Commun 7:1–15. doi:10.1038/ncomms12662

    Google Scholar 

  • Pickles BJ, Egger KN, Massicotte HB, Green DS (2012) Ectomycorrhizas and climate change. Fungal Ecol 5:73–84. doi:10.1016/j.funeco.2011.08.009

    Article  Google Scholar 

  • Plassard C, Dell B (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiol 30:1129–1139. doi:10.1093/treephys/tpq063

    Article  CAS  PubMed  Google Scholar 

  • Power SA, Ashmore MR (1994) Nutrient relations and root mycorrhizal status of healthy and declining beech (Fagus sylvatica L.) in southern Britain. Water Air Soil Pollut 86:317–333

    Article  Google Scholar 

  • Prosser RS, Anderson JC, Hanson ML, Solomon KR, Sibley PK (2016) Indirect effects of herbicides on biota in terrestrial edge-of-field habitats: a critical review of the literature. Agric Ecosyst Environ 232:59–72. doi:10.1016/j.agee.2016.07.009

    Article  CAS  Google Scholar 

  • Ramos MA, Sousa NR, Franco AR, Costa V, Oliveira RS, Castro PML (2013) Effect of diflubenzuron on the development of Pinus pinaster seedlings inoculated with the ectomycorrhizal fungus Pisolithus tinctorius. Environ Sci Pollut Res 20:582–590. doi:10.1007/s11356-012-1056-0

    Article  CAS  Google Scholar 

  • Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210:786–789

    Article  PubMed  Google Scholar 

  • Riah W, Laval K, Laroche-Ajzenberg E, Mougin C, Latour X, Trinsoutrot-Gattin I (2014) Effects of pesticides on soil enzymes: a review. Environ Chem Lett 12:257–273. doi:10.1007/s10311-014-0458-2

    Article  CAS  Google Scholar 

  • Rodriguez JH, Wannaz ED, Salazar MJ, Pignata ML, Fangmeier A, Franzaring J (2012) Accumulation of polycyclic aromatic hydrocarbons and heavy metals in the tree foliage of Eucalyptus rostrata, Pinus radiata and Populus hybridus in the vicinity of a large aluminium smelter in Argentina. Atmos Environ 55:35–42. doi:10.1016/j.atmosenv.2012.03.026

    Article  CAS  Google Scholar 

  • Root RB (1967) The niche exploitation pattern of the Blue-Gray Gnatcatcher. Ecol Monogr 37:317–350. doi:10.2307/1942327

    Article  Google Scholar 

  • Santo-Silva EE, Almeida WR, Tabarelli M, Peres CA (2016) Habitat fragmentation and the future structure of tree assemblages in a fragmented Atlantic forest landscape. Plant Ecol 217:1129–1140. doi:10.1007/s11258-016-0638-1

    Article  Google Scholar 

  • Schimper AFW, Fisher WR (1903) Plant-geography upon a physiological basis. Clarendon Press, Oxford

    Book  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365. doi:10.1093/jexbot/53.372.1351

    PubMed  Google Scholar 

  • Scott PM, Shearer BL, Barber PA, Hardy GESJ (2013) Relationships between the crown health, fine root and ectomycorrhizae density of declining Eucalyptus gomphocephala. Australas Plant Pathol 42:121–131. doi:10.1007/s13313-012-0152-4

    Article  Google Scholar 

  • Seidl R, Thom D, Kautz M, Martin-Benito D, Peltoniemi M, Vacchiano G, Wild J, Ascoli D, Petr M, Honkaniemi J, Lexer MJ, Trotsiuk V, Mairota P, Svoboda M, Fabrika M, Nagel TA, Reyer CPO (2017) Forest disturbances under climate change. Nat Clim Change 7:395–402

    Article  Google Scholar 

  • Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786. doi:10.3389/fpls.2015.00786

    PubMed  PubMed Central  Google Scholar 

  • Stenlid J, Oliva J (2016) Phenotypic interactions between tree hosts and invasive forest pathogens in the light of globalization and climate change. Philos Trans R Soc Lond B. doi:10.1098/rstb.2015.0455

    Google Scholar 

  • Swaty RL, Deckert RJ, Whitham TG, Gehring CA (2004) Ectomycorrhizal abundance and community composition shifts with drought: predictions from tree rings. Ecology 85:1072–1084. doi:10.1890/03-0224

    Article  Google Scholar 

  • Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Chuyong G, Koljalg U (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodologies biases. New Phytol 188:291–301. doi:10.1111/j.1469-8137.2010.03373.x

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A (2014) Global diversity and geography of soil fungi. Science 346:1256688. doi:10.1126/science.1256688

    Article  PubMed  CAS  Google Scholar 

  • Tonn N, Ibáñez I (2016) Plant-mycorrhizal fungi associations along an urbanization gradient: implications for tree seedling survival. Urban Ecosyst. doi:10.1007/s11252-016-0630-5

    Google Scholar 

  • Tracey JA, Bevins SN, VandeWoude S, Crooks KR (2014) An agent-based movement model to assess the impact of landscape fragmentation on disease transmission. Ecosphere 5:1–24. doi:10.1890/ES13-00376.1

    Article  Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. doi:10.1111/j.1469-8137.2004.01159.x

    Article  Google Scholar 

  • Truong C, Mujic AB, Healy R, Kuhar F, Furci G, Torres D, Niskanen T, Sandoval-Leiva PA, Fernández N, Escobar JM, Moretto A, Palfner G, Pfister D, Nouhra E, Swenie R, Sánchez-García M, Matheny PB, Smith ME (2017) How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol 214:913–919. doi:10.1111/nph.14509

    Article  PubMed  Google Scholar 

  • Van der Linde JA, Wingfield MJ, Crous CJ, Six DL, Roux J (2017) Landscape degradation may contribute to large-scale die-offs of Euphorbia ingens in South Africa. S Afr J Bot 111:144–152. doi:10.1016/j.sajb.2017.03.022

    Article  Google Scholar 

  • Vannette RL, Leopold DR, Fukami T (2016) Forest area and connectivity influence root-associated fungal communities in a fragmented landscape. Ecology 97:2374–2383. doi:10.1002/ecy.1472

    Article  PubMed  Google Scholar 

  • Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, Gianinazzi-Pearson V (2013) Mycorrhiza-induced resistance against the root–knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Biochem 60:45–54. doi:10.1016/j.soilbio.2013.01.013

    Article  CAS  Google Scholar 

  • Walker LR, Wardle DA, Bardgett RD, Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98:725–736. doi:10.1111/j.1365-2745.2010.01664.x

    Article  Google Scholar 

  • Wasserman JL, Mineo L, Majumdar SK (1987) Detection of heavy metals in oak mycorrhizae of northeastern Pennsylvania forests, using X-ray microanalysis. Can J Bot 65:2622–2627. doi:10.1139/b87-353

    Article  CAS  Google Scholar 

  • Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312. doi:10.1007/s11104-013-1670-8

    Article  CAS  Google Scholar 

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227. doi:10.1139/b04-082

    Article  Google Scholar 

  • Will RE, Wilson SM, Zou CB, Hennessey TC (2013) Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest–grassland ecotone. New Phytol 200:366–374. doi:10.1111/nph.12321

    Article  PubMed  Google Scholar 

  • Williams A, Hedlund K (2013) Indicators of soil ecosystem services in conventional and organic arable fields along a gradient of landscape heterogeneity in southern Sweden. Appl Soil Ecol 65:1–7. doi:10.1016/j.apsoil.2012.12.019

    Article  Google Scholar 

  • Williams A, Manoharan L, Rosenstock NP, Olsson PA, Hedlund K (2016) Long-term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (Hordeum vulgare) mycorrhizal carbon and phosphorus exchange. New Phytol 213:874–885. doi:10.1111/nph.14196

    Article  PubMed  CAS  Google Scholar 

  • Wright SJ, Duber HC (2001) Poachers and forest fragmentation alter seed dispersal, seed survival, and seedling recruitment in the palm Attalea butyraceae, with implications for tropical tree diversity. Biotropica 33:583–595. doi:10.1646/0006-3606(2001)033[0583:PAFFAS]2.0.CO;2

    Article  Google Scholar 

  • Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625. doi:10.1890/10-1558.1

    Article  PubMed  Google Scholar 

  • Xiao S, Zhang W, Ye Y, Zhao J, Wang K (2017) Soil aggregate mediates the impacts of land uses on organic carbon, total nitrogen, and microbial activity in a Karst ecosystem. Sci Rep 7:41402. doi:10.1038/srep41402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the two anonymous reviewers whose comments greatly improved this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sarah J. Sapsford.

Additional information

Communicated by Martin Nunez.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sapsford, S.J., Paap, T., Hardy, G.E.S.J. et al. The ‘chicken or the egg’: which comes first, forest tree decline or loss of mycorrhizae?. Plant Ecol 218, 1093–1106 (2017). https://doi.org/10.1007/s11258-017-0754-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-017-0754-6

Keywords

Navigation