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Exotic plants accumulate and share herbivores yet dominate communities via rapid growth

  • 1.

    Heger, T. & Jeschke, J. M. The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123, 741–750 (2014).

    Article 

    Google Scholar 

  • 2.

    Elton, C. S. The Ecology of Invasions by Animals and Plants (Springer, 1958).

  • 3.

    Keane, R. M. & Crawley, M. J. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17, 164–170 (2002).

    Article 

    Google Scholar 

  • 4.

    Mitchell, C. E. & Power, A. G. Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627 (2003).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 5.

    Colautti, R. I., Ricciardi, A., Grigorovich, I. A. & MacIsaac, H. J. Is invasion success explained by the enemy release hypothesis? Ecol. Lett. 7, 721–733 (2004).

    Article 

    Google Scholar 

  • 6.

    Liu, H. & Stiling, P. Testing the enemy release hypothesis: a review and meta-analysis. Biol. Invasions 8, 1535–1545 (2006).

    Article 

    Google Scholar 

  • 7.

    Meijer, K., Schilthuizen, M., Beukeboom, L. & Smit, C. A review and meta-analysis of the enemy release hypothesis in plant-herbivorous insect systems. PeerJ 4, e2560v1 (2016).

    Article 

    Google Scholar 

  • 8.

    Jeschke, J. M. & Heger, T. (eds) Invasion Biology: Hypotheses and Evidence (CABI, 2018).

  • 9.

    Levine, J. M., Adler, P. B. & Yelenik, S. G. A meta-analysis of biotic resistance to exotic plant invasions. Ecol. Lett. 7, 975–989 (2004).

    Article 

    Google Scholar 

  • 10.

    Maron, J. L. & Vilà, M. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95, 361–373 (2001).

    Article 

    Google Scholar 

  • 11.

    Callaway, R. M. & Ridenour, W. M. Novel weapons: invasive success and the evolution of increased competitive ability. Front. Ecol. Environ. 2, 436–443 (2004).

    Article 

    Google Scholar 

  • 12.

    Cappuccino, N. & Arnason, J. T. Novel chemistry of invasive exotic plants. Biol. Lett. 2, 189–193 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 13.

    Bezemer, T. M., Harvey, J. A. & Cronin, J. T. Response of native insect communities to invasive plants. Ann. Rev. Entomol. 59, 119–141 (2014).

    CAS 
    Article 

    Google Scholar 

  • 14.

    Keeler, M. S. & Chew, F. S. Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156, 559–568 (2008).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 15.

    Eckberg, J. O., Tenhumberg, B. & Louda, S. M. Insect herbivory and propagule pressure influence Cirsium vulgare invasiveness across the landscape. Ecology 93, 1787–1794 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 16.

    Bürki, C. & Nentwig, W. Comparison of herbivore insect communities of Heracleum sphondylium and H. mantegazzianum in Switzerland (Spermatophyta: Apiaceae). Entomol. Gen. 22, 147–155 (1997).

    Article 

    Google Scholar 

  • 17.

    Cincotta, C. L., Adams, J. M. & Holzapfel, C. Testing the enemy release hypothesis: a comparison of foliar insect herbivory of the exotic Norway maple (Acer platanoides L.) and the native sugar maple (A. saccharum L.). Biol. Invasions 11, 379–388 (2008).

    Article 

    Google Scholar 

  • 18.

    Cronin, J. T., Bhattarai, G. P., Allen, W. J. & Meyerson, L. A. Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96, 1115–1127 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 19.

    Hu, X.-T. & Dong, B.-C. Herbivory and nitrogen availability affect performance of an invader Alternanthera philoxeroides and its native congener A. sessilis. Flora 257, 151412 (2019).

    Article 

    Google Scholar 

  • 20.

    Agrawal, A. A. & Kotanen, P. M. Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol. Lett. 6, 712–715 (2003).

    Article 

    Google Scholar 

  • 21.

    Agrawal, A. A. et al. Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86, 2979–2989 (2005).

    Article 

    Google Scholar 

  • 22.

    Parker, J. D. & Hay, M. E. Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol. Lett. 8, 959–967 (2005).

    Article 

    Google Scholar 

  • 23.

    Parker, J. D., Burkepile, D. E. & Hay, M. E. Opposing effects of native and exotic herbivores on plant invasions. Science 311, 1459–1461 (2006).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 24.

    Parker, I. M. & Gilbert, G. S. When there is no escape: the effects of natural enemies on native, invasive, and non-native plants. Ecology 88, 1210–1224 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 25.

    Dostál, P. et al. Enemy damage of exotic plant species is similar to that of natives and increases with productivity. J. Ecol. 101, 388–399 (2013).

    Article 

    Google Scholar 

  • 26.

    Meijer, K. et al. Phytophagous insects on native and non-native host plants: combining the community approach and the biogeographical approach. PLoS ONE 10, e0125607 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 27.

    Schultheis, E. H., Berardi, A. E. & Lau, J. A. No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96, 2446–2457 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 28.

    Beckstead, J. & Parker, I. M. Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecology 84, 2824–2831 (2003).

    Article 

    Google Scholar 

  • 29.

    van Kleunen, M., Weber, E. & Fischer, M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol. Lett. 13, 235–245 (2010).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 30.

    Ashton, I. W. & Lerdau, M. T. Tolerance to herbivory, and not resistance, may explain differential success of invasive, naturalized, and native North American temperate vines. Divers. Distrib. 14, 169–178 (2008).

    Article 

    Google Scholar 

  • 31.

    Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 14435 (2017).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 32.

    Eppinga, M. B., Rietkerk, M., Dekker, S. C., De Ruiter, P. C. & van der Putten, W. H. Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114, 168–176 (2006).

    Article 

    Google Scholar 

  • 33.

    Bufford, J. L. et al. Taxonomic similarity, more than contact opportunity, explains novel plant–pathogen associations between native and alien taxa. N. Phytol. 212, 657–667 (2016).

    CAS 
    Article 

    Google Scholar 

  • 34.

    White, E. M., Wilson, J. C. & Clarke, A. R. Biotic indirect effects: a neglected concept in invasion biology. Divers. Distrib. 12, 443–455 (2006).

    Article 

    Google Scholar 

  • 35.

    Allen, W. J. in Plant Invasions: The Role of Species Interactions (CABI Publishing, 2020).

  • 36.

    Holt, R. D. Predation, apparent competition, and the structure of prey communities. Theor. Popul. Biol. 12, 197–229 (1977).

    MathSciNet 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 37.

    Holt, R. D. & Bonsall, M. B. Apparent competition. Annu. Rev. Ecol. Evol. Syst. 48, 447–471 (2017).

    Article 

    Google Scholar 

  • 38.

    Sessions, L. & Kelly, D. Predator-mediated apparent competition between an introduced grass, Agrostis capillaris, and a native fern, Botrychium australe (Ophioglossaceae), in New Zealand. Oikos 96, 102–109 (2002).

    Article 

    Google Scholar 

  • 39.

    Dangremond, E. M., Pardini, E. A. & Knight, T. M. Apparent competition with an invasive plant hastens the extinction of an endangered lupine. Ecology 91, 2261–2271 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 40.

    Bhattarai, G. P., Meyerson, L. A. & Cronin, J. T. Geographic variation in apparent competition between native and invasive Phragmites australis. Ecology 98, 349–358 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 41.

    Simberloff, D. & Von Holle, B. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invasions 1, 21–32 (1999).

    Article 

    Google Scholar 

  • 42.

    Allen, W. J. et al. Community-level direct and indirect impacts of an invasive plant favour exotic over native species. J. Ecol. 108, 2499–2510 (2020).

    Article 

    Google Scholar 

  • 43.

    Morris, R. J., Lewis, O. T. & Godfray, C. J. Experimental evidence for apparent competition in a tropical forest food web. Nature 428, 310–313 (2004).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 44.

    Tack, A. J. M., Gripenberg, S. & Roslin, T. Can we predict indirect interactions from quantitative food webs? – an experimental approach. J. Anim. Ecol. 80, 108–118 (2011).

    PubMed 
    Article 

    Google Scholar 

  • 45.

    Frost, C. M. et al. Apparent competition drives community-wide parasitism rates and changes in host abundance across ecosystem boundaries. Nat. Commun. 7, 12644 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 46.

    Bardgett, R. D. & Wardle, D. A. Aboveground–Belowground Linkages: Biotic Interactions, Ecosystem Processes and Global Change (Oxford University Press, 2010).

  • 47.

    Heinen, R., Biere, A., Harvey, J. A. & Bezemer, T. M. Effects of soil organisms on aboveground plant-insect interactions in the field: patterns, mechanisms and the role of methodology. Front. Ecol. Evol. 6, 106 (2018).

    Article 

    Google Scholar 

  • 48.

    Bever, J. D., Westover, K. M. & Antonovics, J. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 85, 561–573 (1997).

    Article 

    Google Scholar 

  • 49.

    Kulmatiski, A., Beard, K. H., Stevens, J. R. & Cobbold, S. M. Plant–soil feedbacks: a meta‐analytical review. Ecol. Lett. 11, 980–992 (2008).

    PubMed 
    Article 

    Google Scholar 

  • 50.

    Levine, J. M., Pachepsky, E., Kendall, B. E., Yelenik, S. G. & Lambers, J. H. Plant-soil feedbacks and invasive spread. Ecol. Lett. 9, 1005–1014 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 51.

    Suding, K. N., Harpole, W. S., Fukami, T., Kulmatiski, A., MacDougall, A. S., Stein, C. & van der Putten, W. H. Consequences of plant–soil feedbacks in invasion. J. Ecol. 101, 298–308 (2013).

    Article 

    Google Scholar 

  • 52.

    Crawford, K. M. et al. When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecol. Lett. 22, 1274–1284 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 53.

    Cornelissen, T., Fernandes, G. W. & Vasconcellos-Neto, J. Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117, 1121–1130 (2008).

    Article 

    Google Scholar 

  • 54.

    Price, P. W. The plant vigor hypothesis and herbivore attack. Oikos 62, 244–251 (1991).

    Article 

    Google Scholar 

  • 55.

    Waller, L. P. et al. Biotic interactions drive ecosystem responses to plant invaders. Science 368, 967–972 (2020).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 56.

    Kozlov, M. V., Lanta, V., Zverev, V. & Zvereva, E. L. Global patterns in background losses of woody plant foliage to insects. Glob. Ecol. Biogeogr. 24, 1126–1135 (2015).

    Article 

    Google Scholar 

  • 57.

    Zas, R., Moreira, X. & Sampedro, L. Tolerance and induced resistance in a native and an exotic pine species: relevant traits for invasion ecology. J. Ecol. 99, 1316–1326 (2011).

    Article 

    Google Scholar 

  • 58.

    Croy, J. R., Meyerson, L. A., Allen, W. J., Bhattarai, G. P. & Cronin, J. T. Lineage and latitudinal variation in Phragmites australis tolerance to herbivory: implications for invasion success. Oikos 129, 1341–1357 (2020).

    Article 

    Google Scholar 

  • 59.

    Liu, G., Huang, Q.-Q., Lin, Z.-G., Huang, F.-F., Liao, H.-X. & Peng, S.-L. High tolerance to salinity and herbivory stresses may explain the expansion of Ipomoea cairica to salt marshes. PLoS ONE 7, e48829 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    Paynter, Q. et al. Why did specificity testing fail to predict the field host-range of the gorse pod moth in New Zealand. Biol. Control 46, 453–462 (2008).

    Article 

    Google Scholar 

  • 61.

    Groenteman, R., Fowler, S. V. & Sullivan, J. J. St. John’s wort beetles would not have been introduced to New Zealand now: a retrospective host range test of New Zealand’s most successful weed biocontrol agents. Biol. Control 57, 50–58 (2011).

    Article 

    Google Scholar 

  • 62.

    Blossey, B. & Nötzold, R. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol. 83, 887–889 (1995).

    Article 

    Google Scholar 

  • 63.

    Felker-Quinn, E., Schweitzer, J. A. & Bailey, J. K. Meta-analysis reveals evolution in invasive plant species but little support for evolution of increased competitive ability (EICA). Ecol. Evol. 3, 739–751 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 64.

    Rotter, M. C. & Holeski, L. M. A meta-analysis of the evolution of increased competitive ability hypothesis: genetic-based trait variation and herbivory resistance trade-offs. Biol. Invasions 20, 2647–2660 (2018).

    Article 

    Google Scholar 

  • 65.

    Shelby, N. et al. No difference in the competitive ability of introduced and native Trifolium provenances when grown with soil biota from their introduced and native ranges. AoB Plants 8, plw016 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 66.

    Harvey, J. A., Bukovinszky, T. & van der Putten, W. H. Interactions between invasive plants and insect herbivores: a plea for a multitrophic perspective. Biol. Conserv. 143, 2251–2259 (2010).

    Article 

    Google Scholar 

  • 67.

    Allen, W. J. et al. Multitrophic enemy release of invasive Phragmites australis and its introduced herbivores in North America. Biol. Invasions 17, 3419–3432 (2015).

    Article 

    Google Scholar 

  • 68.

    Kim, T. N. & Underwood, N. Plant neighborhood effects on herbivory: damage is both density and frequency dependent. Ecology 96, 1431–1437 (2015).

    PubMed 
    Article 

    Google Scholar 

  • 69.

    Bartomeus, I., Vilà, M. & Santamaría, L. Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155, 761–770 (2008).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 70.

    Lekberg, Y., Gibbons, S. M., Rosendahl, S. & Ramsey, P. W. Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J. 7, 1424–1433 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 71.

    Fernandez-Conradi, P., Jactel, H., Robin, C., Tack, A. J. M. & Castagneyrol, B. Fungi reduce preference and performance of insect herbivores on challenged plants. Ecology 99, 300–311 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Reinhart, K. O. & Callaway, R. M. Soil biota and invasive plants. N. Phytol. 170, 445–457 (2006).

    Article 

    Google Scholar 

  • 73.

    Gioria, M. & Osborne, B. A. Resource competition in plant invasions: emerging patterns and research needs. Front. Plant Sci. 5, 501 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 74.

    Frost, C. M. et al. Using ecological network theory to predict biological invasions. Trends Ecol. Evol. 34, 831–843 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 75.

    Sauve, A. M. C., Thébault, E., Pocock, M. J. O. & Fontaine, C. How plants connect pollination and herbivory networks and their contribution to community stability. Ecology 97, 908–917 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 76.

    Pilosof, S., Porter, M. A., Pascual, M. & Kéfi, S. The multilayer nature of ecological networks. Nat. Ecol. Evol. 1, 0101 (2017).

    Article 

    Google Scholar 

  • 77.

    Weir, B. S., Turner, S. J., Silvester, W. B., Park, D. C. & Young, J. M. Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Appl. Environ. Microbiol. 70, 5980–5987 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 78.

    Cappuccino, N. & Carpenter, D. Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol. Lett. 1, 435–438 (2005).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 79.

    Liu, H., Stiling, P. & Pemberton, R. W. Does enemy release matter for invasive plants? evidence from a comparison of insect herbivore damage among invasive, non-invasive and native congeners. Biol. Invasions 9, 773–781 (2007).

    Article 

    Google Scholar 

  • 80.

    Howell, C. Consolidated List of Environmental Weeds in New Zealand. DOC Research & Development Series 292 (Department of Conservation, 2008).

  • 81.

    Ghanizadeh, H. & Harrington, K. C. Weed management in New Zealand pastures. Agronomy 9, 448 (2019).

    CAS 
    Article 

    Google Scholar 

  • 82.

    Kos, M., Tuijl, M. A. B., de Roo, J., Mulder, P. P. J. & Bezemer, T. M. Species-specific plant–soil feedback effects on aboveground plant-insect interactions. J. Ecol. 103, 904–914 (2015).

    CAS 
    Article 

    Google Scholar 

  • 83.

    Heinen, R., Biere, A. & Bezemer, T. M. Plant traits shape soil legacy effects on individual plant–insect interactions. Oikos 129, 261–273 (2020).

    CAS 
    Article 

    Google Scholar 

  • 84.

    Bezemer, T. M et al. Above‐and below‐ground herbivory effects on below‐ground plant–fungus interactions and plant–soil feedback responses. J. Ecol. 101, 325–333 (2013).

    Article 
    CAS 

    Google Scholar 

  • 85.

    Heinze, J., Wacker, A. & Kulmatiski, A. Plant–soil feedback effects altered by aboveground herbivory explain plant species abundance in the landscape. Ecology 101, e03023 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 86.

    Müller, C. B., Adriaanse, I. C. T., Belshaw, R. & Godfray, H. C. J. The structure of an aphid-parasitoid community. J. Anim. Ecol. 68, 346–370 (1999).

    Article 

    Google Scholar 

  • 87.

    R Core Team. R: a language and environment for statistical computing. Version 3.6.1. R Foundation for Statistical Computing http://www.R-project.org (2019).

  • 88.

    Bates, D. et al. lme4: linear mixed-effects models using ‘Eigen’ and S4. R package version 1.1-21 http://CRAN.R-project.org/package=lme4 (2019).

  • 89.

    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. emmeans: estimated marginal means, aka least-squares means. R package version 1.3.5.1 http://CRAN.R-project.org/package=emmeans (2019).

  • 90.

    Dormann, C. F., Fruend, J. & Gruber, B. bipartite: visualising bipartite networks and calculating some (ecological) indices. R package version 2.13 http://CRAN.R-project.org/package=bipartite (2019).


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