Abstract
The novel associations between invasive plants and their natural enemies in the introduced range have recently received increasing attention; however, the effects of novel enemies on exotic plant performance and competition with native species remain poorly explored. Here, we tested the impact of herbivory by a native beetle, Cassida piperata, on the performance of the exotic species Alternanthera philoxeroides and competition with a native congener, Alternanthera sessilis, using common garden experiments in central China. We found A. philoxeroides was able to fully compensate for intense herbivory by C. piperata. Herbivory by C. piperata that released at the average density in this region had no impact on competition between the native and exotic plant species. Our results indicate that herbivory by novel enemies may not reduce exotic plant performance due to plant compensation. However, high tolerance to herbivory may not confer a competitive advantage for exotic species compared to less tolerant native competitors if the herbivore damage is below a certain threshold. Thus, it is necessary to assess the impact of novel enemies on exotic plant performance and competition with native plants along gradients of insect densities. This may lead to a better understanding of how best to exploit the role of native herbivores in facilitating or slowing plant invasions.
Similar content being viewed by others
References
Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715. doi:10.1046/j.1461-0248.2003.00498.x
Bertheau C, Brockerhoff EG, Roux-Morabito G, Lieutier F, Jactel H (2010) Novel insect-tree associations resulting from accidental and intentional biological ‘invasions’: a meta-analysis of effects on insect fitness. Ecol Lett 13:506–515. doi:10.1111/j.1461-0248.2010.01445.x
Bossdorf O, Prati D, Auge H, Schmid B (2004) Reduced competitive ability in an invasive plant. Ecol Lett 7:346–353. doi:10.1111/j.1461-0248.2004.00583.x
Callaway RM, Newingham B, Zabinski CA, Mahall BE (2001) Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbours. Ecol Lett 4:429–433. doi:10.1046/j.1461-0248.2001.00251.x
Chun YJ, Kleunen MV, Dawson W (2010) The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance. Ecol Lett 13:937–946. doi:10.1111/j.1461-0248.2010.01498.x
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733. doi:10.1111/j.1461-0248.2004.00616.x
Dai H, Lu X, Zhang J, Ding J (2013) Responses of a native beetle to novel exotic plant species with varying invasion history. Ecol Entomol 39:118–124. doi:10.1111/een.12072
Gendron AD, Marcogliese DJ, Thomas M (2012) Invasive species are less parasitized than native competitors, but for how long? The case of the round goby in the Great Lakes-St. Lawrence Basin. Biol Invasions 14:367–384. doi:10.1007/s10530-011-0083-y
Julien MH, Skarratt B, Maywald GF (1995) Potential geographical distribution of alligator weed and its biological control by Agasicles hygrophila. J Aquat Plant Manage 33:55–60
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. doi:10.1016/S0169-5347(02)02499-0
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. doi:10.1007/s11258-012-0073-x
Lin G, Yang Y, Hu J (1990) Studies on biology and control of Alternanthera philoxeroides. J Jiangsu Agric Coll 11:57–63 (in Chinese)
Lu X-M, Ding J (2010) Flooding compromises compensatory capacity of an invasive plant: implications for biological control. Biol Invasions 12:179–189. doi:10.1007/s10530-009-9441-4
Lu X, Ding J (2012) History of exposure to herbivores increases the compensatory ability of an invasive plant. Biol Invasions 14:649–658. doi:10.1007/s10530-011-0106-8
Lu X, Dai H, Ding J (2010) Con-specific neighbours may enhance compensation capacity in an invasive plant. Plant Biol 12:445–452. doi:10.1111/j.1438-8677.2009.00247.x
Lu X-M, Siemann E, Shao X, Wei H, Ding J-Q (2013) Climate warming affects biological invasions by shifting interactions of plants and herbivores. Glob Change Biol 19:2339–2347. doi:10.1111/gcb.12244
Ma R-Y. 2001 Ecological adaptation for the introduced biocontrol agent, Agasicles hygropghila, for Alligatorweed, Alternanthera philoxeroides, in China. PhD Thesis, Chinese Academy of Agricultural Sciences, Beijing, p 120 (in Chinese)
Mao R, Lu X, Ding J (2011) Effects of a nematode Meloidogyne incognita and its interaction with above-ground herbivory on an invasive wetland plant, alligator weed (Alternanthera philoxeroides). Plant Spec Biol 26:73–83. doi:10.1111/j.1442-1984.2010.00309.x
Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373. doi:10.1034/j.1600-0706.2001.950301.x
Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. Am Nat 134:1–19. doi:10.1086/284962
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. doi:10.1371/journal.pone.0017227
Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Annu Rev Entomol 36:511–534. doi:10.1146/annurev.en.36.010191.002455
Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422. doi:10.1016/j.tree.2004.05.010
Oksanen L, Fretwell SD, Arruda J, Niemela P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261. doi:10.1086/283817
Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967. doi:10.1111/j.1461-0248.2005.00799.x
Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461. doi:10.1126/science.1121407
Pearson DE, Potter T, Maron JL (2012) Biotic resistance: exclusion of native rodent consumers releases populations of a weak invader. J Ecol 100:1383–1390. doi:10.1111/j.1365-2745.2012.02025.x
Persson I-L, Danell K, Bergström R (2005) Different moose densities and accompanied changes in tree morphology and browse production. Ecol Appl 15:1296–1305. doi:10.1890/04-0499
Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Evol S 18:209–235. doi:10.1146/annurev.es.18.110187.001233
Sainty G, McCorkelle G, Julien M (1998) Control and spread of alligator weed Alternanthera philoxeroides (Mart.) Griseb., in Australia: lessons for other regions. Wetl Ecol Manage 5:195–201. doi:10.1023/A:1008248921849
Schooler SS, Yeates AG, Wilson JRU, Julien MH (2007) Herbivory, mowing, and herbicides differently affect production and nutrient allocation of Alternanthera philoxeroides. Aquat Bot 86:62–68
Siemann E, Rogers WE, Dewalt SJ (2006) Rapid adaptation of insect herbivores to an invasive plant. Proc R Soc Lond B Biol Sci 273:2763–2769. doi:10.1098/rspb.2006.3644
Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185. doi:10.1016/S0169-5347(98)01576-6
Sun Y, Ding J, Frye MJ (2010) Effects of resource availability on tolerance of herbivory in the invasive Alternanthera philoxeroides and the native Alternanthera sessilis. Weed Res 50:527–536. doi:10.1111/j.1365-3180.2010.00822.x
Tang Y-G (1994) Study on the bionomies of Cassida piperata Hope (Coleoptera: Cassididae). Entomol Knowl 31:158–160 (in Chinese)
Tiffin P, Inouye BD (2000) Measuring tolerance to herbivory: accuracy and precision of estimates made using natural versus imposed damage. Evolution 54:1024–1029. doi:10.1111/j.0014-3820.2000.tb00101.x
Verhoeven KJF, Biere A, Harvey JA, van der Putten WH (2009) Plant invaders and their novel natural enemies: who is naïve? Ecol Lett 12:107–117. doi:10.1111/j.1461-0248.2008.01248.x
Wilson JRU, Yeates A, Schooler S, Julien MH (2007) Rapid response to shoot removal by the invasive wetland plant, alligator weed (Alternanthera philoxeroides). Environ Exp Bot 60:20–25. doi:10.1016/j.envexpbot.2006.06.003
Acknowledgments
We would like to thank Wenfeng Guo, Hongjun Dai, Yan Sun, and Sunliang Feng for their field and laboratory assistance. This work was funded by the Knowledge Innovation Program of the Chinese Academy of Sciences and the National Science Foundation of China (31100302 and 31370547) while preparing this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Martin Nunez.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lu, X., Shao, X. & Ding, J. No impact of a native beetle on exotic plant performance and competitive ability due to plant compensation. Plant Ecol 215, 275–284 (2014). https://doi.org/10.1007/s11258-014-0296-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-014-0296-0