Abstract
During introduction, invasive plants can be released from specialist herbivores, but may retain generalist herbivores and encounter novel enemies. For fast-growing invasive plants, tolerance of herbivory via compensatory regrowth may be an important defense against generalist herbivory, but it is unclear whether tolerance responses are specifically induced by different herbivores and whether specificity differs among native and invasive plant populations. We conducted a greenhouse experiment to examine the variation among native and invasive populations of Chinese tallow tree, Triadica sebifera, in their specificity of tolerance responses to herbivores by exposing plants to herbivory from either one of two generalist caterpillars occurring in the introduced range of Triadica. Simultaneously, we measured the specificity of another defensive trait, extrafloral nectar (EFN) production, to detect potential tradeoffs between resistance and tolerance of herbivores. Invasive populations had higher aboveground biomass tolerance than native populations, and responded non-specifically to either herbivore, while native populations had significantly different and specific aboveground biomass responses to the two herbivores. Both caterpillar species similarly induced EFN in native and invasive populations. Plant tolerance and EFN were positively correlated or had no relationship and biomass in control and herbivore-damaged plants was positively correlated, suggesting little costs of tolerance. Relationships among these vegetative traits depended on herbivore type, suggesting that some defense traits may have positive associations with growth-related processes that are differently induced by herbivores. Importantly, loss of specificity in invasive populations indicates subtle evolutionary changes in defenses in invasive plants that may relate to and enhance their invasive success.
Similar content being viewed by others
References
Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432. doi:10.1111/j.1365-2435.2010.01796.x
Agrawal AA, Fishbein M (2008) Phylogenetic escalation and decline of plant defense strategies. Proc Natl Acad Sci USA 105:10057–10060. doi:10.1073/pnas.0802368105
Agrawal AA, Salminen JP, Fishbein M (2009) Phylogenetic trends in phenolic metabolism of milkweeds (Asclepias): evidence for escalation. Evolution 63:663–673. doi:10.1111/j.1558-5646.2008.00573.x
Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302. doi:10.1111/j.1558-5646.2008.00573.x
Belsky AJ, Carson WP, Jensen CL, Fox GA (1993) Overcompensation by plants—herbivore optimization or red herring. Evol Ecol 7:109–121. doi:10.1007/BF01237737
Bergman M (2002) Can saliva from moose, Alces alces, affect growth responses in the sallow, Salix caprea? Oikos 96:164–168. doi:10.1034/j.1600-0706.2002.960118.x
Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889. doi:10.2307/2261425
Boalt E, Lehtilä K (2007) Tolerance to apical and foliar damage: costs and mechanisms in Raphanus raphanistrum. Oikos 116:2071–2081. doi:10.1111/j.2007.0030-1299.16056.x
Bruce K, Cameron G, Harcombe PA, Jubinsky G (1997) Introduction, impact on native habitats, and management of a woody invader, the Chinese tallow tree, Sapium sebiferum (L) Roxb. Natural Areas J 17:255–260
Carmona D, Fornoni J (2013) Herbivores can select for mixed defensive strategies in plants. New Phytol 197:576–585. doi:10.1111/nph.12023
Carrillo J, Wang Y, Ding J, Klootwyk K, Siemann E (2012a) Decreased indirect defense in the invasive tree, Triadica sebifera. Plant Ecol 213:945–954. doi:10.1007/s11258-012-0055-z
Carrillo J, Wang Y, Ding J, Siemann E (2012b) Induction of extrafloral nectar depends on herbivore type in invasive and native Chinese tallow seedlings. Basic Appl Ecol 13:449–457. doi:10.1016/j.baae.2012.07.006
Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25:399–407. doi:10.1111/j.1365-2435.2010.01805.x
Franklin MT, Ritland CE, Myers JH (2010) Spatial and temporal changes in genetic structure of greenhouse and field populations of cabbage looper, Trichoplusia ni. Mol Ecol 19:1122–1133. doi:10.1111/j.1365-294X.2010.04548.x
Garrido E, Andraca-Gómez G, Fornoni J (2012) Local adaptation: simultaneously considering herbivores and their host plants. New Phytol 193:445–453. doi:10.1111/j.1469-8137.2011.03923
Gavloski JE, Lamb RJ (2000) Compensation for herbivory in cruciferous plants: specific responses to three defoliating insects. Environ Entomol 29:1258–1267. doi:10.1603/0046-225X-29.6.1258
Greenberg SM, Sappington TW, Legaspi BC, Liu TX, Setamou M (2001) Feeding and life history of Spodoptera exigua (Lepidoptera : Noctuidae) on different host plants. Ann Entomol Soc Am 94:566–575. doi:10.1603/0013-8746(2001)094[0566:FALHOS]2.0.CO;2
Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61. doi:10.1111/j.1469-8137.2007.02330.x
Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:61–67. doi:10.1016/S1360-1385(01)02186-0
Heil M, Fiala B, Baumann B, Linsenmair KE (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct Ecol 14:749–757. doi:10.1046/j.1365-2435.2000.00480.x
Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Natl Acad Sci USA 98:1083–1088. doi:10.1073/pnas.98.3.1083
Hochwender CG, Cha DH, Czesak ME, Fritz RS, Smyth RR, Kaufman AD, Warren B, Neumann A (2012) Protein storage and root:shoot reallocation provide tolerance to damage in a hybrid willow system. Oecologia 169:49–60. doi:10.1007/s00442-011-2176-9
Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98:1157–1167. doi:10.1111/j.1365-2745.2010.01704.x
Huang W, Carrillo J, Ding J, Siemann E (2012) Interactive effects of herbivory and competition intensity determine invasive plant performance. Oecologia 170:373–382. doi:10.1007/s00442-012-2328-6
Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714. doi:10.1111/j.1461-0248.2005.00769.x
Lankau RA, Rogers WE, Siemann E (2004) Constraints on the utilisation of the invasive Chinese tallow tree Sapium sebiferum by generalist native herbivores in coastal prairies. Ecol Entomol 29:66–75. doi:10.1111/j.0307-6946.2004.00575.x
Leimu R, Koricheva J (2006) A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112:1–9. doi:10.1111/j.0030-1299.2006.41023.x
Lennartsson T, Tuomi J, Nilsson P (1997) Evidence for an evolutionary history of overcompensation in the grassland biennial Gentianella campestris (Gentianaceae). Am Nat 149:1147–1155. doi:10.1086/286043
Manzaneda AJ, Prasad KV, Mitchell-Olds T (2010) Variation and fitness costs for tolerance to different types of herbivore damage in Boechera stricta genotypes with contrasting glucosinolate structures. New Phytol 188:464–477. doi:10.1111/j.1469-8137.2010.03385.x
Mitchel ER (1979) Migration by Spodoptera exigua and S. frugiperda, North America style. In: Rabb Rl, Kenneday GG (eds) Movement of highly mobile insects: concepts and methodology in research. North Carolina State University, Raleigh, pp 386-393
Mondor EB, Addicott JF (2003) Conspicuous extra-floral nectaries are inducible in Vicia faba. Ecol Lett 6:495–497. doi:10.1046/j.1461-0248.2003.00457.x
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
Núñez-Farfán J, Fornoni J, Luis Valverde P (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566. doi:10.1146/annurev.ecolsys.38.091206.095822
Oduor AM, Lankau RA, Strauss SY, Gomez JM (2011) Introduced Brassica nigra populations exhibit greater growth and herbivore resistance but less tolerance than native populations in the native range. New Phytol 191:536–544. doi:10.1111/j.1469-8137.2011.03685.x
Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459. doi:10.1146/annurev-ento-112408-085333
Pilson D (2000) The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evol Ecol 14:457–489. doi:10.1023/A:1010953714344
Shorey HH, Andres LA, Hale RL (1962) The biology of Trichoplusia ni (Lepidoptera: Noctuidae). I. Life history and behavior. Ann Entomol Soc Am 55:591–597
Siemann E, Rogers WE (2003) Herbivory, disease, recruitment limitation and success of alien and native tree species. Ecology 84:1489–1505. doi:10.1890/0012-9658(2003)084[1489:HDRLAS]2.0.CO;2
Siemann E, Rogers W, Dewalt S (2006) Rapid adaptation of insect herbivores to an invasive plant. Proc R Soc B 273:2763–2769. doi:10.1098/rspb 2006.3644
Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37. doi:10.1111/j.1365-2745.2004.00962.x
Stevens MT, Waller DM, Lindroth RL (2007) Resistance and tolerance in Populus tremuloides: genetic variation, costs, and environmental dependency. Evol Ecol 29:829–847. doi:10.1007/s10682-006-9154-4
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
Tiffin P, Rausher MD (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am Nat 154:700–716. doi:10.1086/303271
Wang Y, Huang W, Siemann E, Zou J, Wheeler G, Carrillo J, Ding J (2011) Lower resistance and higher tolerance of invasive host plants: biocontrol agents reach high densities but exert weak control. Ecol Appl 21:729–738. doi:10.1890/09-2406.1
Wang Y, Siemann E, Wheeler GS, Zhu L, Gu X, Ding J (2012) Genetic variation in anti-herbivore chemical defences in an invasive plant. J Ecol 100:894–904. doi:10.1111/j.1365-2745.2012.01980.x
Wang Y, Carrillo J, Siemann G, Wheeler GS, Zhu L, Gu X, Ding J (2013) Specificity of extrafloral nectar induction by herbivores differs among native and invasive populations of tallow tree. Ann Bot. doi:10.1093/aob/mct129
Zhang Z, Wang SP, Jiang GM, Patton B, Nyren P (2007) Responses of Artemisia frigida Willd. (Compositae) and Leymus chinensis (Trin.) Tzvel. (Poaceae) to sheep saliva. J Arid Environ 70:111–119. doi:10.1016/j.jaridenv.2006.12.002
Zou J, Rogers WE, Siemann E (2008) Increased competitive ability and herbivory tolerance in the invasive plant Sapium sebiferum. Biol Invasions 10:291–302. doi:10.1007/s10530-007-9130-0
Acknowledgments
We thank J. Ding for constructive comments and support from an Alliance for Graduate Education and the Professoriate, Ford Foundation, and American Association of University Women fellowship (J. Carrillo), the US National Science Foundation (DEB 0820560; E. Siemann), and the foreign visiting professorship of the Chinese Academy of Sciences (2009S1-30; E. Siemann).
Conflict of interest
The authors declare they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Martin Heil.
J. Carrillo and D. McDermott are co-first authors.
The experiment conducted herein complied with the current laws of the country in which they were performed (USA).
Rights and permissions
About this article
Cite this article
Carrillo, J., McDermott, D. & Siemann, E. Loss of specificity: native but not invasive populations of Triadica sebifera vary in tolerance to different herbivores. Oecologia 174, 863–871 (2014). https://doi.org/10.1007/s00442-013-2807-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-013-2807-4