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Release from below- and aboveground natural enemies contributes to invasion success of a temperate invader

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Abstract

Aims

Efforts to concurrently test for enemy release of both above- and belowground enemies for invasive plants in non-native range are limited. Moreover, direct evidence for the causal link between enemy release and performance is rare for invasive plants. Thus, we sought to investigate if above- and/or belowground enemies are involved in the enemy release mechanisms at various life stages of a temperate invader and their consequences on plant community properties.

Methods

We conducted field surveys of enemy damage and plant performance, and plant-soil feedback experiments in the glasshouses using Ambrosia trifida in both its non-native and native ranges across the seed, seedling, and adult life stages.

Results

Field surveys showed that seeds of A. trifida were more severely damaged by aboveground enemies in the native relative to the non-native range, while the difference in leaf damage between ranges was small. Plant-soil feedback experiments showed that release from belowground enemies was also important, as seed germination and plant growth were significantly reduced in soils from the native range compared with soils from the non-native range. Consistent with the above results, A. trifida was larger, produced more seeds, had higher density, and exerted stronger impacts on co-occurring native plants in the non-native relative to the native range.

Conclusion

Our results demonstrated that release from both above- and belowground enemies at various life stages contributed to the invasion success of A. trifida in its non-native range and highlighted the importance of considering both above- and belowground enemy release when studying plant invasions.

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References

  • Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86:2979–2989

    Google Scholar 

  • Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25(8):468–478

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Blumenthal D, Mitchell CE, Pyšek P, Jarošík V (2009) Synergy between pathogen release and resource availability in plant invasion. Proc Natl Acad Sci U S A 106:7899–7904

    PubMed  PubMed Central  CAS  Google Scholar 

  • Brinkman EP, Van der Putten WH, Bakker E-J, Verhoeven KJF (2010) Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073

    Google Scholar 

  • Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733

    PubMed  CAS  Google Scholar 

  • Callaway RM, Bedmar EJ, Reinhart KO, Silvan CG, Klironomos J (2011) Effects of soil biota from different ranges on Robinia invasion: acquiring mutualists and escaping pathogens. Ecology 92:1027–1035

    PubMed  Google Scholar 

  • Chen H-S, Guo W, Min L, Guo J-Y, Luo Y-H, Zhou Z-S (2013) A field test of joint control of the alien invasive weed Ambrosia artemisiifolia with Ophraella communa and Epiblema strenuana. Chin J Biol Control 29:362–369

    CAS  Google Scholar 

  • Chen L, Swenson NG, Ji N, Mi X, Ren H, Guo L, Ma K (2019) Differential soil fungus accumulation and density dependence of trees in a subtropical forest. Science 366(6461):124–128

    PubMed  CAS  Google Scholar 

  • Daws MI, Hall J, Flynn S, Pritchard HW (2007) Do invasive species have bigger seeds? Evidence from intra- and inter-specific comparisons. S Afr J Bot 73:138–143

    Google Scholar 

  • Dawson W (2015) Release from belowground enemies and shifts in root traits as interrelated drivers of alien plant invasion success: a hypothesis. Ecol Evol 5:4505–4516

    PubMed  PubMed Central  Google Scholar 

  • Dewalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483

    Google Scholar 

  • Dostálek T, Münzbergová Z, Kladivová A, Macel M (2016) Plant-soil feedback in native vs. invasive populations of a range expanding plant. Plant Soil 399:209–220

    Google Scholar 

  • Ebeling SK, Hensen I, Auge H (2008) The invasive shrub Buddleja davidii performs better in its introduced range. Divers Distrib 14:225–233

    Google Scholar 

  • Engelkes T, Morrien E, Verhoeven KJF, Bezemer TM, Biere A, Harvey JA, McIntyre LM, Tamis WLM, van der Putten WH (2008) Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456:946–948

    PubMed  CAS  Google Scholar 

  • Fan S, Yu H, Dong X, Wang L, Chen X, Yu D, Liu C (2016) Invasive plant Alternanthera philoxeroides suffers more severe herbivory pressure than native competitors in recipient communities. Sci Rep UK 6:36542

    CAS  Google Scholar 

  • Feng Y-L, Lei Y-B, Wang R-F, Callaway RM, Valiente-Banuet A, Inderjit LY-P, Zheng Y-L (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci U S A 106:1853–1856

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gard B, Bretagnolle F, Dessaint F, Laitung B (2013) Invasive and native populations of common ragweed exhibit strong tolerance to foliar damage. Basic Appl Ecol 14:28–35

    Google Scholar 

  • Gundale MJ, Paul K, Marie-Charlotte N, Urban N, Lucas RW, Wardle DA (2014) Interactions with soil biota shift from negative to positive when a tree species is moved outside its native range. New Phytol 202:415–421

    PubMed  Google Scholar 

  • Huang K, Kong D-L, Lu X-R, Feng W-W, Liu M-C, Feng Y-L (2020) Lesser leaf herbivore damage and structural defenses and greater nutrient concentrations for invasive alien plants: evidence from 47 pairs of invasive and non-invasive plants. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2020.137829

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    PubMed  CAS  Google Scholar 

  • Kwong RM, Sagliocco JL, Harms NE, Butler KL, Martine GD, Green PT (2019) Could enemy release explain invasion success of Sagittaria platyphylla in Australia and South Africa? Aquat Bot 153:67–72

    Google Scholar 

  • Li Y-P, Feng Y-L, Barclay G (2012) No evidence for evolutionarily decreased tolerance and increased fitness in invasive Chromolaena odorata: implications for invasiveness and biological control. Plant Ecol 213:1157–1166

    Google Scholar 

  • Li M, Huo X-H, Song W-F, Wang B-F, Li B-Y, Zhang D (2014) Research advances on the invasive plant, Ambrosia trifida. J Weed Sci 32:33–37

    CAS  Google Scholar 

  • Liang M, Liu X, Parker IM, Johnson D, Zheng Y, Luo S, Gilbert GS, Yu S (2019) Soil microbes drive phylogenetic diversity-productivity relationships in a subtropical forest. Sci Adv 5(10):eaax5088

    PubMed  PubMed Central  CAS  Google Scholar 

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

    Google Scholar 

  • MacDonald AAM, Kotanen PM (2010) Leaf damage has weak effects on growth and fecundity of common ragweed (Ambrosia artemisiifolia). Botany 88:158–164

    Google Scholar 

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

    Google Scholar 

  • Meijer K, Schilthuizen M, Beukeboom L, Smit C (2016) A review and meta-analysis of the enemy release hypothesis in plant-herbivorous insect systems. Peer J 4:e2778

    PubMed  Google Scholar 

  • Meng L, Li B-P (2006) Mating and oviposition behaviors of exotic leafbeetle, Ophraella communa. Chin Bull Entomol 43:806–809

    Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    PubMed  CAS  Google Scholar 

  • Morrison WE, Hay ME (2011) Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PLoS One 6:e17227

    PubMed  PubMed Central  CAS  Google Scholar 

  • Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967

    Google Scholar 

  • Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457

    PubMed  Google Scholar 

  • Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008) Plant–soil–microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781

    PubMed  Google Scholar 

  • Sun B, Li JD (2005) Research advance on control of ragweed. Res Agr Modernization 26:317–320

    Google Scholar 

  • Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190

    Google Scholar 

  • Urli M, Brown CD, Perez RN, Chagnon PL, Vellend M (2016) Increased seedling establishment via enemy release at the upper elevational range limit of sugar maple. Ecology 97:3058–3069

    PubMed  Google Scholar 

  • Vasquez EC, Meyer GA (2011) Relationships among leaf damage, natural enemy release, and abundance in exotic and native prairie plants. Biol Invasions 13:621–633

    Google Scholar 

  • Vermeij MJA, Smith TB, Dailer ML, Smith CM (2009) Release from native herbivores facilitates the persistence of invasive marine algae: a biogeographical comparison of the relative contribution of nutrients and herbivory to invasion success. Biol Invasions 11:1463–1474

    Google Scholar 

  • Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708

    PubMed  Google Scholar 

  • Wang Y (2014) A comparative study of defense and competitiveness capability among three invasive plants. Master degree thesis, Shenyang Agricultural University, Shenyang, Liaoning, China

  • Wang J, Lv GZ, Jiang H, Sun XD, Zhao ZH, Zhou P (2013) Research advance on invasive alien species Ambrosia trifida Linn. J Anhui Agric Sci 41(1533–1536):1556

    Google Scholar 

  • Wei S, Qu Z, Zhang C, Li Y, Li X (2006) Invasive alien species giant ragweed (Ambrosia trifida L.) and its risk assessment. Plant Prot 32:14–19

    Google Scholar 

  • Yin PP, Li JD, Yin H, Sun B, Sun JN, Wang GJ, Yan XF (2010) Impacts of Ambrosia trifida invasion on plant biodiversity. J Northwest A and F Univ 38:190–194

    Google Scholar 

  • Zheng Y-L, Feng Y-L, Zhang L-K, Callaway RM, Valiente-Banuet A, Luo D-Q, Liao Z-Y, Lei Y-B, Barclay GF, Silva-Pereyra C (2015) Integrating novel chemical weapons and evolutionarily increased competitive ability in success of a tropical invader. New Phytol 205:1350–1359

    PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Xin-Rui Li and Zi-Wei Huang for the helpful assistance in field measurements and also to three anonymous reviewers and the handling editor, Dr. Kenny Png, for their valuable comments on earlier versions of this paper.

Funding

This study was supported by the National Key R&D Program of China (2017YFC1200101), the National Natural Science Foundation of China (31971557, 31670545, 31870522, and 31470575), China Scholarship Council, and the innovative talents for colleges and universities of Liaoning Province (LR2016048).

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Author notes

  1. Yuan-Zheng Zhao and Ming-Chao Liu contributed equally to this work.

Authors and Affiliations

  1. Liaoning Key Laboratory for Biological Invasions and Global Changes, Shenyang Agricultural University, Shenyang, 110866, Liaoning Province, China

    Yuan-Zheng Zhao, Ming-Chao Liu, Yu-Long Feng, Wei-Wei Feng, Xiu-Rong Lu, Shuo Wang, Xiao-Lin Wei & De-Liang Kong

  2. Department of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, 010018, Inner Mongolia, China

    Dong Wang

  3. Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA, 70118, USA

    Keith Clay

  4. Department of Biology, Indiana University, Bloomington, IN, 47405, USA

    Lekeah A. Durden

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  1. Yuan-Zheng Zhao
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Contributions

YLF and YZZ designed the study. YZZ, MCL, DW, WWF, LAD, XRL, SW, and XLW collected the data. YYZ, YLF, and MCL conducted the data analyses. YZZ wrote the first draft of the manuscript. YLF, KC, and DLK contributed to the results, analyses, writing, and revisions.

Corresponding authors

Correspondence to Yu-Long Feng or De-Liang Kong.

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Responsible Editor: Kenny Png.

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Zhao, YZ., Liu, MC., Feng, YL. et al. Release from below- and aboveground natural enemies contributes to invasion success of a temperate invader. Plant Soil 452, 19–28 (2020). https://doi.org/10.1007/s11104-020-04520-5

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