Plant Ecology and Evolution 154(2): 161-172, doi: 10.5091/plecevo.2021.1805
An experimental investigation of costs of tolerance against leaf and floral herbivory in the herbaceous weed horsenettle (Solanum carolinense, Solanaceae)
expand article infoMichael J. Wise, Erika L. Mudrak§
‡ Department of Biology, Roanoke College, 221 College Ave., Salem, VA, 24153, United States of America§ Blandy Experimental Farm, University of Virginia, Boyce, United States of America
Open Access

Background and aims – A plant’s tolerance of herbivory depends on its ability to endure and compensate for damage so as to lessen the impact that herbivores have on the plant’s performance (e.g. its growth, reproduction, or fitness). While tolerance of herbivory is beneficial to plants, it is rarely complete, and individuals in plant populations tend to vary in their levels of tolerance. The goal of this study was to investigate potential costs associated with tolerance of leaf and floral herbivory in horsenettle (Solanum carolinense), a perennial herbaceous weed that is often subjected to high levels of damage from a diversity of herbivores.

Material and methods – We exposed 96 potted individuals across eight genets of horsenettle to factorial treatments of leaf herbivory by lace bugs and simulated floral herbivory by weevils. We quantified tolerance for each plant genet for both types of herbivory in terms of the impact of damage on the number of flowers opened, number of seeds produced, and root biomass (i.e. paternal, maternal, and vegetative tolerance, respectively).

Key results – Plant genets ranged widely in their ability to compensate for leaf and flower damage. While there was little evidence for tradeoffs in tolerance through the different routes, there was strong evidence of tradeoffs in genets’ abilities to tolerate herbivore damage to leaves and damage to flowers.

Conclusion – Tolerance is a useful defence strategy to cope with damage caused by herbivores, but its evolution may be constrained by concomitant costs and tradeoffs. The evolutionary role of the tradeoffs identified in this study are likely to be greater the more species of herbivores a plant hosts, and the more that herbivore levels vary both spatially and temporally.

Anthonomus nigrinus, costs of tolerance, florivory, folivory, Gargaphia solani, horsenettle, Solanum carolinense, tolerance of herbivory, tradeoffs


  • Avila-Sakar G. 2020. Resource allocation and defense against herbivores in wild and model plants. In: Núñez-Farfán J. & Valverde P.L. (eds) Evolutionary ecology of plant-herbivore interaction: 37–61. Springer Nature Switzerland AG, Cham, Switzerland.
  • Bardner R. & Fletcher K.E. 1974. Insect infestations and their effects on the growth and yield of field crops: a review. Bulletin of Entomological Research 64: 141–160.
  • Bassett I.J. & Munro D.B. 1986. The biology of canadian weeds. 78. Solanum carolinense L. and Solanum rostratum Dunal. Canadian Journal of Plant Science 66: 977–991.
  • Carmago I.D. 2020. Toward a unifying quest for an understanding of tolerance mechamisms to herbivore damage and its eco-evolutionary dynamics. In: Núñez-Farfán J. & Valverde P.L. (eds) Evolutionary ecology of plant-herbivore interaction: 63–86. Springer Nature Switzerland AG, Cham, Switzerland.
  • Chittenden F.H. 1895. The potato-bud weevil. Insect Life 7: 350–352
  • Dahlgren E. & Lehtilä K. 2015. Tolerance to apical and leaf damage of Raphanus raphanistrum in different competitive regimes. Ecology and Evolution 5: 5193–5202.
  • Elle E. & Meagher T.R. 2000. Sex allocation and reproductive success in the andromonoecious perennial Solanum carolinense (Solanaceae). II. Paternity and functional gender. The American Naturalist 156: 622–636.
  • Fineblum W.L. & Rausher M.D. 1995. Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377: 517–520.
  • Fornoni J., Núñez-Farfán J. & Valverde P.L. 2003. Evolutionary ecology of tolerance to herbivory: advances and perspectives. Comments on Theoretical Biology 8: 643–663.
  • Fornoni J., Valverde P.L. & Núñez-Farfán J. 2004. Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution 58: 1696–1704.
  • Garcia L.C. & Eubanks M.D. 2019. Overcompensation for insect herbivory: a review and meta-analysis of the evidence. Ecology 100: e02585.
  • Garrido E., Llamas-Guzmán L.P. & Fornoni J. 2016. The effect of frequency-dependent selection on resistance and tolerance to herbivory. Journal of Evolutionary Biology 29: 483–489.
  • Gómez J.M. & Fuentes M. 2001. Compensatory responses of an arid land crucifer, Chorispora tenella (Brassicaceae), to experimental flower removal. Journal of Arid Environments 49: 855–863.
  • Hakes A.S. & Cronin J.T. 2011. Resistance and tolerance to herbivory in Solidago altissima (Asteraceae): genetic variability, costs, and selection for multiple traits. American Journal of Botany 98: 1446–1455.
  • Hendrix S.D. 1984. Reactions of Heracleum lanatum to floral herbivory by Depressaria pastinacella. Ecology 65: 191–197.
  • Hendrix S.D. & Trapp E.J. 1981. Plant-herbivore interactions: insect induced changes in host plant sex expression and fecundity. Oecologia 49: 119–122.
  • Hochwender C.G., Marquis R.J. & Stowe K.A. 2000. The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca. Oecologia 122: 361–370.
  • Ilnicki R.D., Tisdell T.F., Fertig S.N. & Furrer A.H. Jr. 1962. Life history studies as related to weed control in the northeast – horse nettle. Bulletin 368. Agricultural Experimental Station, University of Rhode Island, Kingston, RI.
  • Juenger T. & Bergelson J. 2000. The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution 54: 764–777.
  • Juenger T. & Lennartsson T. 2000. Tolerance in plant ecology and evolution: toward a more unified theory of plant-herbivore interaction. Evolutionary Ecology 14: 283–287.
  • König M.A.E., Lehtilä K., Wiklund C. & Ehrlén J. 2014. Among-population variation in tolerance to larval herbivory by Anthocharis cardamines in the polyploid herb Cardamine pratensis. PLoS ONE 9: e99333.
  • Krupnick G.A. & Weis A.E. 1998. Floral herbivore effect on the sex expression of an andromonoecious plant, Isomeris arborea (Capparaceae). Plant Ecology 134: 151–162.
  • Lehtilä K. 1999. Impact of herbivore tolerance and resistance on plant life histories. In: Vuorisalo T.O. & Mutikainen P.K. (eds) Life history evolution in plants: 303–328. Kluwer Academic Publishers, Dordrecht.
  • 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.
  • Manzaneda A.J., Prasad K.V.S.K. & 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 Phytologist 188: 464–477.
  • Mauricio R., Rausher M.D. & Burdick D.S. 1997. Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78: 1301–1311. fwkv9x
  • NAPPO 2003. Pra/grains panel facts sheet – Solanum carolinense L. North American Plant Protection Organization, Ottawa.
  • Nihranz C.T., Walker W.S., Brown S.J., Mescher M.C., De Moraes C.M. & Stephenson A.G. 2020. Transgenerational impacts of herbivory and inbreeding on reproductive output in Solanum carolinense. American Journal of Botany 107: 1–12.
  • Painter R.H. 1958. Resistance of plants to insects. Annual Review of Entomology 3: 267–290.
  • Pearse I.S., Aguilar J., Schroder J. & Strauss S.Y. 2017. Macroevolutionary constraints to tolerance: trade-offs with drought tolerance and phenology, but not resistance. Ecology 98: 2758–2772. /
  • Pilson D. 2000. The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evolutionary Ecology 14: 457–489.
  • Richman A.D., Kao T.-H., Schaeffer S.W. & Uyenoyama M.K. 1995. S-allele sequence diversity in natural populations of Solanum carolinense (horsenettle). Heredity 75: 405–415.
  • Scholes D.R., Rasnick E.N. & Paige K.N. 2017. Characterization of Arabidopsis thaliana regrowth patterns suggests a trade-off between undamaged fitness and damage tolerance. Oecologia 184: 643–652. /
  • Solomon B.P. 1985. Environmentally influenced changes in sex expression in an andromonoecious plant. Ecology 66: 1321–1332.
  • Stephenson A.G. 1992. The regulation of maternal investment in plants. In: Marshall C. & Grace J. (eds) Fruit and seed production. Aspects of development, environmental physiology and ecology: 151–171. Cambridge University Press, Cambridge, UK.
  • Steven J.C., Peroni P.A. & Rowell E. 1999. The effects of pollen addition on fruit set and sex expression in the andromonoecious herb horsenettle (Solanum carolinense). The American Midland Naturalist 141: 247–252. c56rdg
  • Stinchcombe J.R. & Rausher M.D. 2002. The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores. Proceedings of the Royal Society of London B. 269: 1241–1246.
  • Strauss S.Y., Watson W. & Allen M.T. 2003. Predictors of male and female tolerance to insect herbivory in Raphanus raphanistrum. Ecology 84: 2074–2082.
  • Tallamy D.W. & Denno R.F. 1982. Life history trade-offs in Gargaphia solani (Hemiptera: Tingidae): the cost of reproduction. Ecology 63: 616–620.
  • Tiffin P. & Rausher M.D. 1999. Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. The American Naturalist 154: 700–716.
  • Turley N.E., Godfrey R.M. & Johnson M.T.J. 2013. Evolution of mixed strategies of plant defense against herbivores. New Phytologist 197: 359–361.
  • Tuttle D.M. 1956. Notes on the life history of seven species of Anthonomus occurring in illinois (Curculionidae, Coleoptera). Annals of the Entomological Society of America 49: 170–173.
  • Wise M.J. 2007a. Evolutionary ecology of resistance to herbivory: an investigation of potential genetic constraints in the multiple-herbivore community of Solanum carolinense. New Phytologist 175: 773–784.
  • Wise M.J. 2007b. The herbivores of horsenettle, Solanum carolinense, in northern Virginia: natural history and damage assessment. Southeastern Naturalist 6: 505–522. fgntq5
  • Wise M.J. 2010. Diffuse interactions between two herbivores and constraints on the evolution of resistance in horsenettle (Solanum carolinense). Arthropod-Plant Interactions 4: 159–164.
  • Wise M.J. 2018. The notoriously destructive potato stalk borer (Trichobaris trinotata) has negligible impact on its native host, Solanum carolinense (horsenettle). Arthropod-Plant Interactions 12: 385–394.
  • Wise M.J. & Abrahamson W.G. 2017. Constraints of the evolution of resistance to gall flies in Solidago altissima: resistance sometimes costs more than it is worth. New Phytologist 215: 423–433.
  • Wise M.J. & Cummins J.J. 2002. Nonfruiting hermaphroditic flowers as reserve ovaries in Solanum carolinense. The American Midland Naturalist 148: 236–245. btggvk
  • Wise M.J. & Cummins J.J. 2007. Herbivory as an agent of natural selection for floral-sex ratio in horsenettle (Solanum carolinense). Evolutionary Ecology Research 9: 1319–1328.
  • Wise M.J. & Hébert J.B. 2010. Herbivores exert natural selection for floral-sex ratio in a field population of horsenettle, Solanum carolinense. Ecology 91: 937–943.
  • Wise M.J. & Rausher M.D. 2013. Evolution of resistance to a multiple-herbivore community: genetic correlations, diffuse coevolution, and constraints on the plant’s response to selection. Evolution 67: 1767–1779.
  • Wise M.J. & Sacchi C.F. 1996. Impact of two specialist insect herbivores on reproduction of horse nettle, Solanum carolinense. Oecologia 108: 328–337.
  • Wise M.J., Abrahamson W.G. & Landis K. 2006. Edaphic environment, gall midges, and goldenrod clonal expansion in a mid-successional old-field. Acta Oecologica 30: 365–373.
  • Wise M.J., Cummins J.J. & De Young C. 2008. Compensation for floral herbivory in Solanum carolinense: identifying mechanisms of tolerance. Evolutionary Ecology 22: 19–37.