Abstract
Non-native plants often dominate novel habitats where they did not co-evolve with the local species. The novel weapons hypothesis suggests that non-native plants bring competitive traits against which native species have not adapted defenses. Novel weapons may directly affect plant competitors by inhibiting germination or growth, or indirectly by attacking competitor plant mutualists (degraded mutualisms hypothesis). Japanese knotweed (Fallopia japonica) and European buckthorn (Rhamnus cathartica) are widespread plant invaders that produce potent secondary compounds that negatively impact plant competitors. We tested whether their impacts were consistent with a direct effect on the tree seedlings (novel weapons) or an indirect attack via degradation of seedling mutualists (degraded mutualism). We compared recruitment and performance using three Ulmus congeners and three Betula congeners treated with allelopathic root macerations from allopatric and sympatric ranges. Moreover, given that the allelopathic species would be less likely to degrade their own fungal symbiont types, we used arbuscular mycorrhizal (AMF) and ectomycorrhizal (ECM) tree species to investigate the effects of F. japonica (no mycorrhizal association) and Rhamnus cathartica (ECM association) on the different fungal types. We also investigated the effects of F. japonica and R. cathartica exudates on AMF root colonization. Our results suggest that the allelopathic plant exudates impact seedlings directly by inhibiting germination and indirectly by degrading fungal mutualists. Novel weapons inhibited allopatric seedling germination but sympatric species were unaffected. However, seedling survivorship and growth appeared more dependent on mycorrhizal fungi, and mycorrhizal fungi were inhibited by allopatric species. These results suggest that novel weapons promote plant invasion by directly inhibiting allopatric competitor germination and indirectly by inhibiting mutualist fungi necessary for growth and survival.
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References
Aguilar-Chama A, Guevara R (2012) Mycorrhizal colonization does not affect tolerance to defoliation of an annual herb in different light availability and soil fertility treatments but increases flower size in light-rich environments. Oecologia 168:131–139
Atkinson MD (1992) Betula Pendula Roth (B. Verrucosa Ehrh.) and B. Pubescens Ehrh. J Ecol 80:837–870
Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380
Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304
Bu R, He HS, Hu Y, Chang Y, Larsen DR (2008) Using the LANDIS model to evaluate forest harvesting and planting strategies under possible warming climates in Northeastern China. For Ecol Manag 254:407–419
Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:1547–1556
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443
Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055
Cantor A, Hale A, Aaron J, Traw MB, Kalisz S (2011) Low allelochemical concentrations detected in garlic mustard-invaded forest soils inhibit fungal growth and AMF spore germination. Biol Invasions 13:3015–3025
Cipollini K, Titus K, Wagner C (2012) Allelopathic effects of invasive species (Alliaria petiolata, Lonicera maackii, Ranunculus ficaria) in the Midwestern United States. Allelopath J 29:63–75
Coyle BF, Sharik TL, Feret PP (1982) Variation in leaf morphology among disjunct and continuous populations of river birch (Betula nigra). Silvae Genet 31:122–125
Dallali S, Lahmayer I, Mokni R, Marichali A, Ouerghemmi S (2014) Phytotoxic effects of volatile oil from Verbena spp. on the germination and radicle growth of wheat, maize, linseed and canary grass and phenolic content of aerial parts. Allelopath J 34:95–105
Duke SO, Dayan FE (2006) Modes of action of phytotoxins from plants. In: Reigosa MJ, Pedrol N, Gonzalez L (eds) Allelopathy: a physiological process with ecological implications. Springer, Dordrecht
Fox J, Weisberg S (2011) An R companion to applied regression. Sage, Thousand Oaks
Gange AC, Smith AK (2005) Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecol Entomol 30:600–606
Godwin H (1943) Rhamnaceae. J Ecol 31:66–92
Hale AN, Kalisz S (2012) Perspectives on allelopathic disruption of plant mutualisms: a framework for individual- and population-level fitness consequences. Plant Ecol 213:1991–2006
Hasan HAH (1998) Studies on toxigenic fungi in roasted foodstuff (salted seed) and halotolerant activity of emodin-producing Aspergillus wentii. Folia Microbiol 43:383–391
Herrera MA, Salamanca CP, Barea JM (1993) Inoculation of woody legumes with selected arbuscular mycorrhizal fungi and rhizobia to recover desertified mediterranean ecosystems. Appl Environ Microbiol 59:129–133
Inderjit Seastedt TR, Callaway RM, Kaur J (2008) Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol Invasions 10:875–890
Inoue M, Nishimura H, Li HH, Mizutani J (1992) Allelochemicals from Polygonum sachalinense Fr. Schm. (Polygonaceae). J Chem Ecol 10:1833–1840
Izhaki I (2002) Emodin—a secondary metabolite with multiple ecological functions in higher plants. New Phytol 155:205–217
Janos DP (1980) Mycorrhizae influence tropical succession. Biotropica 12:56–64
Jessing KK, Duke O, Cedergreen N (2014) Potential ecological roles of artemisinin produced by Artemisia annua L. J Chem Ecol 40:100–117
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
Klionsky SM, Amatangelo KL, Waller DM (2011) Above- and belowground impacts of European buckthorn (Rhamnus cathartica) on four native forbs. Restor Ecol 19:728–737
Klironomos J (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
Koide RT, Dickie IA (2002) Effects of mycorrhizal fungi on plant populations. Plant Soil 244:307–317
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103
Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. R Soc 270:775–781
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Mallik AU, Pellissier F (2000) Effects of Vaccinium myrtillus on spruce regeneration: testing the notion of coevolutionary significance of allelopathy. J Chem Ecol 26:2197–2209
Malloch DW, Pirozynski KA, Raven PH (1980) Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (a review). Proc Natl Acad Sci 77:2113–2118
Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501
Mitchell CE, Power AG (2006) Disease dynamics in plant communities. In: Collinge S, Ray C (eds) Disease ecology: community structure and pathogen dynamics. Oxford University Press, New York
Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422
Nantel P, Neumann P (1992) Ecology of ectomycorrhizal-basidiomycete communities on a local vegetation gradient. Ecology 73:99–117
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
R Core Team Version 3.3.2 (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rabotnov T (1982) Importance of the evolutionary approach to the study of allelopathy. Sov J Ecol 12:127–130
Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569
Requena N, Jeffries P, Barea JM (1996) Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl Environ Microbiol 62:842–847
Schnitzer A, Muller S (1998) Ecology and biogeography of highly invasive plants in Europe: giant knotweeds from Japan (Fallopia japonica and F-sachalinensis). Revue d’écologie 53:3–38
Schreiner RP, Koide RT (1993) Antifungal compounds from the roots of mycotrophic and non-mycotrophic plant-species. New Phytol 123:99–105
Sera B (2012) Effects of soil substrate contaminated by knotweed leaves on seed development. Pol J Environ Stud 21:713–717
Serniak LT (2016) Comparison of the allelopathic effects and uptake of Fallopia japonica phytochemicals by Raphanus sativus. Weed Res 56:97–101
Siqueira J, Saggin-Junior OJ (2001) Dependency on arbuscular mycorrhizal fungi and responsiveness of some Brazilian native woody species. Mycorrhiza 11:245–255
Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13
Spector T, Putz FE (2006) Biomechanical plasticity facilitates invasion of maritime forests in the southern USA by Brazilian pepper (Schinus terebinthifolius). Biol Invasions 8:255–260
Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731
Stinson K, Kaufman S, Durbin L, Lowenstein F (2007) Impacts of garlic mustard invasion on a forest understory community. Northeast Nat 14:73–88
Trial H Jr, Diamond JB (1979) Emodin in buckthorn: a feeding deterrent to phytophagous insects. Can Entomol 111:207–212
Tsahar E, Friedman J, Izhaki I (2002) Impact on fruit removal and seed predation of a secondary metabolite, emodin, in Rhamnus alaternus fruit pulp. Oikos 99:290–299
Varga S, Kytoviita M-M (2010) Gender dimorphism and mycorrhizal symbiosis affect floral visitors and reproductive output in Geranium sylvaticum. Funct Ecol 24:750–758
Vierheilig H, Bennett R, Kiddle G, Kaldorf M, Ludwig-Muller J (2000) Differences in glucosinolate patterns and arbuscular mycorrhizal status of glucosinolate-containing plant species. New Phytol 146:343–352
Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399–407
Warren RJ II, Labatore AC, Candeias M (2017) Allelopathic invasive tree (Rhamnus cathartica) alters native plant communities. Plant Ecol 218:1233–1241
Acknowledgements
We thank Dr. James Berry at the University of Buffalo for use of the Dorsheimer Laboratory/Greenhouse. We also thank two anonymous reviewers for helpful comments that improved the manuscript.
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The data generated and analyzed for the current study are available in the SUNY Buffalo State Digital Commons [http://digitalcommons.buffalostate.edu].
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PP conceived the ideas and designed methodology; PP collected the data; PP and RW analyzed the data; PP and RW led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Communicated by William E. Rogers.
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Pinzone, P., Potts, D., Pettibone, G. et al. Do novel weapons that degrade mycorrhizal mutualisms promote species invasion?. Plant Ecol 219, 539–548 (2018). https://doi.org/10.1007/s11258-018-0816-4
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DOI: https://doi.org/10.1007/s11258-018-0816-4