Of mutualism and migration: will interactions with novel ericoid mycorrhizal communities help or hinder northward Rhododendron range shifts?

Afkhami M, McIntyre P, Strauss S (2014) Mutualist-mediated effects on species’ range limits across large geographic scales. Ecol Lett 17(10):1265–1273. https://doi.org/10.1111/ele.12332 Baer KC, Maron JL (2018) dispersal seed predation and pollen limitation constrain population growth across the geographic distribution of Astragalus utahensis. J Ecol 106(4):1646–1659. https://doi.org/10.1111/1365-2745.12932 Bellemare J, Moeller D (2014) Climate change and forest herbs of temperate deciduous forests. In: Gilliam FS, Roberts MR (eds) The herbaceous layer in forests of Eastern North America. Oxford University Press, New York, pp 460–479. https://doi.org/10.1093/acprof:osobl/9780199837656.003.0021 Bellemare J, Connolly B, Sax DF (2017) Climate change, managed relocation, and the risk of intra-continental plant invasions: a theoretical and empirical exploration relative to the flora of New England. Rhodora 119:73–109. https://doi.org/10.3119/16-10 Benning JW, Moeller DA (2019) Maladaptation beyond a geographic range limit driven by antagonistic and mutualistic biotic interactions across an abiotic gradient. Evolution 73:2044–2059. https://doi.org/10.1111/evo.13836 Benning JW, Eckhart VM, Geber MA, Moeller DA (2019) Biotic interactions contribute to the geographic range limit of an annual plant : herbivory and phenology mediate fitness beyond a range margin. Am Nat 193(6):786–797. https://doi.org/10.1086/7031878 Bidartondo MI, Bruns TD (2005) On the origins of extreme mycorrhizal specificity in the Monotropoideae (Ericaceae): performance trade-offs during seed germination and seedling development. Mol Ecol 14:1549–1560. https://doi.org/10.1111/j.1365-294X.2005.02503.x Brodie JF, Lieberman S, Moehrenschlager A, Redford KH, Rodríguez JP, Schwartz M, Watson JEM (2021) Global policy for assisted colonization of species. Science 372:456–458. https://doi.org/10.1126/science/abg0532 Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54(4):735–740. https://doi.org/10.1046/j.1351-0754.2003.0555.x Case TJ, Taper ML (2000) Interspecific competition, environmental gradients, gene flow, and the coevolution of species’ borders. Am Nat 155(5):583–605. https://doi.org/10.1086/303351 Chen I, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species of climate warming. Science 333(6045):1024–1027. https://doi.org/10.1126/science.1206432 Corlett RT, Westcott DA (2013) Will plant movements keep up with climate change? Trends Ecol Evol 28(8):482–488. https://doi.org/10.1016/j.tree.2013.04.003 David AS, Quintana-Ascencio PF, Menges ES, Thapa-Magar KB, Afkhami ME, Searcy CA (2019) Soil microbiomes underlie population persistence of an endangered plant species. Am Nat. https://doi.org/10.1086/704684 Dearnaley JDW (2007) Further advances in orchid mycorrhizal research. Mycorrhiza 17(6):475–486. https://doi.org/10.1007/s00572-007-0138-1 Delavaux CS, Weigelt P, Dawson W, Bever JD (2019) Mycorrhizal fungi influence global plant biogeography. Nat Ecol Evol 3:424–429. https://doi.org/10.1038/s41559-019-0823-4 Diffenbaugh NS (2013) Changes in ecologically critical terrestrial climate conditions. Science 341:496–481. https://doi.org/10.1126/science.1237123 Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proc R Soc B 276:3037–3045. https://doi.org/10.1098/rspb.2009.0413 Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40(1):677–697. https://doi.org/10.1146/annurev.ecolsys.110308.120159 Erfmeier A, Bruelheide H (2004) Comparison of native and invasive Rhododendron ponticum populations: growth, reproduction and morphology under field conditions. Flora 199:120–133. https://doi.org/10.1078/0367-2530-00141 Franklin J, Miller JA (2010) Mapping species distributions: spatial inference and prediction. Cambridge University Press, New York. https://doi.org/10.1017/CBO9780511810602 Gardner RO, Early JW (1996) The naturalisation of banyan figs (Ficus spp., Moraceae) and their pollinating wasps (Hymenoptera: Agaonidae) in New Zealand. NZ J Bot 34(1):103–110. https://doi.org/10.1080/0028825X.1996.10412697 Gravel D, Massol F, Mouillot D, Mouquet N (2011) Trophic theory of island biogeography. Ecol Lett 14:1010–1016. https://doi.org/10.1111/j.1461-0248.2011.01667.x Grelet GA, Meharg AA, Duff EI, Anderson IC, Alexander IJ (2009) Small genetic differences between ericoid mycorrhizal fungi affect nitrogen uptake by Vaccinium. New Phytol 181(3):708–718. https://doi.org/10.1111/j.1469-8137.2008.02678.x Grossenbacher D, Runquist RB, Goldberg EE, Brandvain Y (2015) Geographic range size is predicted by plant mating system. Ecol Lett 18:706–713. https://doi.org/10.1111/ele.12449 Haines A (2011) Flora Novae Angliae. Yale University Press, New Haven Hille Ris Lambers J, Harsch MA, Ettinger AK, Ford KR, Theobald EJ (2013) How will biotic interactions influence climate change-induced range shifts? Ann NY Acad Sci 1297:112–125. https://doi.org/10.1111/nyas.12182 Hochberg ME, Ives AR (1999) Can natural enemies enforce geographical range limits? Ecography 22(3):268–276. https://doi.org/10.1111/j.1600-0587.1999.tb00502.x Hoeksema JD (2010) Ongoing coevolution in mycorrhizal interactions. New Phytol 187(2):286–300. https://doi.org/10.1111/j.1469-8137.2010.03305.x Jacquemyn H, Merckx V, Brys R, Tyteca D, Cammue BPA, Honnay O, Lievens B (2011) Analysis of network architecture reveals phylogenetic constraints on mycorrhizal specificity in the genus Orchis (Orchidaceae). New Phytol 192:518–528. https://doi.org/10.1111/j.1469-8137.2011.03796.x Jansa J, Vosátka M (2000) In vitro and post vitro inoculation of micropropagated Rhododendrons with ericoid mycorrhizal fungi. Appl Soil Ecol 15(2):125–136. https://doi.org/10.1016/S0929-1393(00)00088-3 Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135(4):575–586. https://doi.org/10.1046/j.1469-8137.1997.00729.x Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107(5):2093–2098. https://doi.org/10.1073/pnas.0906710107 Kartesz JT (2014) and continuously updated. The Biota of North America Program (BONAP). North American Plant Atlas. (http://www.bonap.org/napa.html). Chapel Hill, N.C. [maps generated from Kartesz, J.T. 2014. Floristic Synthesis of North America, Version 1.0. Biota of North America Program (BONAP). (in press)] Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17(4):164–170. https://doi.org/10.1016/S0169-5347(02)02499-0 Kerley SJ, Read DJ (1998) The biology of mycorrhiza in the Ericaceae- XX- Plant and mycorrhizal necromass as nitrogenous substrates for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host. New Phytol 139:353–360. https://doi.org/10.1046/j.1469-8137.1998.00189.x Klironomos J (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84(9):2292–2301. https://doi.org/10.1890/02-0413 Lankau R (2016) Ectomycorrhizal fungal richness declines towards the host species’ range edge. Mol Ecol 25:3224–3241. https://doi.org/10.1111/mec.13628 Lankau RA, Keymer DP (2018) Simultaneous adaptation and maladaptation of tree populations to local rhizosphere microbial communities at different taxonomic scales. New Phytol 217:1267–1278. https://doi.org/10.1111/nph.14911 Lin L, Lee M, Chen J (2011) Decomposition of organic matter by the ericoid mycorrhizal endophytes of Formosan rhododendron (Rhododendron formosanum Hemsl.). Mycorrhiza 21:331–339. https://doi.org/10.1007/s00572-010-0342-2 Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion Ecology. Wiley-Blackwell, Hoboken Louthan AM, Doak DF, Angert AL (2015) Where and when do species interactions set range limits? Trends Ecol Evol 30(12):780–792. https://doi.org/10.1016/j.tree.2015.09.011 Malloch DW, Pirozynskit KA, Ravent PH (1980) Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants. Proc Natl Acad Sci 77(4):2113–2118. https://doi.org/10.1073/pnas.77.4.2113 Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466(7307):752–755. https://doi.org/10.1038/nature09273 McLachlan JS, Hellmann JJ, Schwartz MW (2007) A framework for debate of assisted migration in an era of climate change. Conserv Biol 21(2):297–302. https://doi.org/10.1111/j.1523-1739.2007.00676.x Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421(6923):625–627. https://doi.org/10.1038/nature01317 Moeller DA, Geber MA, Eckhart VM (2012) Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology 93(5):1036–1048. https://doi.org/10.1890/11-1462.1 Moyano J, Dickie IA, Rodriguez-Cabal M, Nuñez MA (2020) Patterns of plant naturalization show that facultative mycorrhizal plants are more likely to succeed outside their native Eurasian ranges. Ecography 43:648–659. https://doi.org/10.1111/ecog.04877 Nadel H, Frank JH, Knight RJ (1992) Escapees and accomplices: the naturalization of exotic Ficus and their associated faunas in Florida. Fla Entomol 75:29–38. https://doi.org/10.2307/3495478 Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90(9):2352–2359. https://doi.org/10.1890/08-2139.1 Osborne OG, De-kayne R, Bidartondo MI, Hutton I, Baker WJ, Turnbull CGN, Savolainen V (2018) Arbuscular mycorrhizal fungi promote coexistence and niche divergence of sympatric palm species on a remote oceanic island. New Phytologyst 217:1254–1266. https://doi.org/10.1111/nph.14850 Parker M (2001) Mutualism as a constraint on invasion success for legumes and rhizobia. Divers Distrib 7:125–136. https://doi.org/10.1046/j.1472-4642.2001.00103.x Parker MA, Malek W, Parker IM (2006) Growth of an invasive legume is symbiont limited in newly occupied habitats. Divers Distrib 12:563–571. https://doi.org/10.1111/j.1366-9516.2006.00255.x Perotto S, Martino E, Abbà S, Vallino M (2012) Genetic diversity and functional aspects of ericoid mycorrhizal fungi. In: Esser K, Hock B (eds) The mycota: (IX) fungal associations, 2nd edn. Springer, Berlin Heidelberg, Berlin, pp 255–285 Policelli N, Bruns TD, Vilgalys R, Nuñez MA (2018) Suilloid fungi as global drivers of pine invasions. New Phytol 222:714–725. https://doi.org/10.1111/nph.15660 Read D (1996) The Structure and function of the ericoid mycorrhizal root. Ann Bot 77(4):365–374. https://doi.org/10.1006/anbo.1996.0044 Rúa MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit LJ, Hoeksema JD (2016) Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16(1):122. https://doi.org/10.1186/s12862-016-0698-9 Schaefer H, Hardy OJ, Silva L, Barraclough TG, Savolainen V (2011) Testing Darwin’s naturalization hypothesis in the Azores. Ecol Lett 14(4):389–396. https://doi.org/10.1111/j.1461-0248.2011.01600.x Seliger BJ, McGill BJ, Svenning JC, Gill JL (2021) Widespread underfilling of the potential ranges of North American trees. J Biogeogr 48(2):359–371. https://doi.org/10.1111/jbi.14001 Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Williams SE (2004) Extinction risk from climate change. Nature 427(6970):145–148. https://doi.org/10.1038/nature02121 Thompson JN, Cunningham BM (2002) Geographic structure and dynamics of coevolutionary selection. Nature 417(6890):735–738. https://doi.org/10.1038/nature00810 Tian W, Zhang CQ, Qiao P, Milne R (2010) Diversity of culturable ericoid mycorrhizal fungi of Rhododendron decorum in Yunnan China. Mycologia 103(4):703–709. https://doi.org/10.3852/10-296 Trevors J (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26:53–59. https://doi.org/10.1016/0167-7012(96)00843-3 Van Der Heijden MGA, Martin FM, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.13288 Van Der Putten WH (2012) Climate change, aboveground-belowground interactions, and species’ range shifts. Annu Rev Ecol Evol Syst 43:365–383. https://doi.org/10.1146/annurev-ecolsys-110411-160423 Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64(12):5004–5007 Wei X, Chen J, Zhang C, Pan D (2016) Differential gene expression in Rhododendron fortunei roots colonized by an ericoid mycorrhizal fungus and increased nitrogen absorption and plant growth. Front Plant Sci 7:1–13. https://doi.org/10.3389/fpls.2016.01594 Zahra S, Novotny V, Fayle TM (2021) Do reverse Janzen-Connell effects reduce species diversity? Trends Ecol Evol 36(5):387–390. https://doi.org/10.1016/j.tree.2021.02.002