Abstract
Spatial variation in biotic interactions and natural selection are fundamental parts of natural systems, and can be driven by differences in both trait distributions and the local environmental context of the interaction. Most studies of plant–animal interactions have been performed only in natural settings, making it difficult to disentangle the effects of traits and context. To assess the relative importance of trait differences and environmental context for among-population variation in plant resistance to herbivory, we compared oviposition by the butterfly Anthocharis cardamines on two ploidy types of the herb Cardamine pratensis under experimentally controlled conditions with oviposition in natural populations. Under controlled conditions, plants from octoploid populations were significantly more preferred than plants from tetraploid populations. This difference was largely mediated by differences in flower size. Among natural populations, there was no difference in oviposition rates between the two ploidy types. Our results suggest that differences in oviposition rates among populations of the two cytotypes in the field are caused mainly by differences in environmental context, and that the higher attractiveness of octoploids to herbivores observed under common environmental conditions is balanced by the fact that they occur in habitats which harbor lower densities of butterflies. This illustrates that spatial variation in biotic interactions is the net result of differences in trait distributions of the interacting organisms and differences in environmental context, and that variation in both traits and context are important in understanding species interactions.
Similar content being viewed by others
References
Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500. doi:10.1034/j.1600-0706.2000.890308.x
Agrawal AA, Lau JA, Hambäck PA (2006) Community heterogeneity and the evolution of interactions between plants and insect herbivores. Q Rev Biol 81:349–376. doi:10.1086/511529
Agrawal AA, Ackerly DD, Adler F, Arnold AE, Cáceres C, Doak DF, Post E, Hudson PJ, Maron J, Mooney KA, Power M, Schemske D, Stachowicz J, Strauss S, Turner MG, Werner E (2007) Filling key gaps in population and community ecology. Front Ecol Environ 5:145–152. doi:10.1890/1540-9295(2007)5[145:FKGIPA]2.0.CO;2
Arvanitis L, Wiklund C, Ehrlén J (2007) Butterfly seed predation: effects of landscape characteristics, plant ploidy level and population structure. Oecologia 152:275–285. doi:10.1007/s00442-007-0659-5
Arvanitis L, Wiklund C, Ehrlén J (2008) Plant ploidy level influences selection by butterfly seed predators. Oikos 117:1020–1025. doi:10.1111/j.2008.0030-1299.16347.x
Arvanitis L, Wiklund C, Münzbergova Z, Dahlgren JP, Ehrlén J (2010) Novel antagonistic interactions associated with plant polyploidization influence trait selection and habitat preference. Ecol Lett 13:130–337. doi:10.1111/j.1461-0248.2009.01429.x
Benkman CW, Holimon WC, Smith JW (2001) The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55:282–294. doi:10.1111/j.0014-3820.2001.tb01293.x
Carmona D, Lajeunesse MJ, Johnson TJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367. doi:10.1111/j.1365-2435.2010.01794.x
Chickering DM (2002) Learning equivalence classes of bayesian-network structures. J Mach Learn Res 2:445–498
Cleland EE, Chuine I, Menzel A, Mooney HA, Schwarts MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365. doi:10.1016/j.tree.2007.04.003
Courtney SP (1981) Coevolution of Pierid butterflies and their cruciferous foodplants III. Anthocharis cardamines (L.) survival, development and oviposition on different host plants. Oecologia 51:91–96. doi:10.1007/BF00344658
Courtney SP (1982) Coevolution of Pierid butterflies and their cruciferous foodplants IV. crucifer apparency and Anthocharis cardamines (L.) oviposition. Oecologia 52:258–265. doi:10.1007/BF00363846
Courtney SP, Courtney S (1982) The ‘edge effect’ in butterfly oviposition: causality in Anthocharis cardamines and related species. Ecol Entomol 7:131–137
Courtney SP, Duggan AE (1983) The population biology of the orange tip butterfly Anthocharis cardamines in Britain. Ecol Entomol 8:271–281. doi:10.1111/j.1365-2311.1983.tb00508.x
Dempster JP (1992) Evidence of an oviposition-deterring pheromone in the orange-tip butterfly, Anthocharis cardamines (L). Ecol Entomol 17:83–85. doi:10.1111/j.1365-2311.1992.tb01043.x
Dempster JP (1997) The role of larval food resources and adult movement in the population dynamics of the orange-tip butterfly (Anthocharis cardamines). Oecologia 111:549–556. doi:10.1007/s004420050270
Duggan AE (1985) Pre-dispersal seed predation by Anthocharis cardamines (Pieridae) in the population dynamics of the perennial Cardamine pratensis (Brassicaceae). Oikos 44:99–106. doi:10.2307/3544049
Ehrendorfer F (1980) Polyploidy and distribution. In: Lewis WH (ed) Polyploidy. Plenum, New York, pp 45–60
Fox J (2006) Teacher’s corner: structural equation modeling with the sem package in R. Struct Equ Modeling 13:465–486. doi:10.1207/s15328007sem1303_7
Gross N, Kunstler G, Liancourt P, de Bello F, Nash Suding K, Lavorel S (2009) Linking individual response to biotic interactions with community structure: a trait-based framework. Funct Ecol 23:1167–1178. doi:10.1111/j.1365-2435.2009.01591.x
Halverson K, Heard SB, Nason JD, Stireman JO III (2008) Differential attack on diploid, tetraploid, and hexaploid Solidago altissima L. by five insect gallmakers. Oecologia 154:755–761. doi:10.1007/s00442-007-0863-3
Husband BC (2000) Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proc R Soc Lond B 267:217–223. doi:10.1098/rspb.2000.0990
Husband BC, Sabara HA (2003) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytol 161:703–713. doi:10.1046/j.1469-8137.2003.00998.x
Husband BC, Schemske DW (2000) Ecological mechanisms of reproductive isolation between diploid and tetraploid Chamerion angustifolium. J Ecol 88:689–701. doi:10.1046/j.1365-2745.2000.00481.x
Janz N, Thompson JN (2002) Plant polyploidy and host expansion in an insect herbivore. Oecologia 130:570–575. doi:10.1007/s00442-001-0832-1
Lehtonen P, Helander M, Wink M, Sporer F, Saikkonen K (2005) Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant. Ecol Lett 8:1256–1263. doi:10.1111/j.1461-0248.2005.00834.x
Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122:1–25. doi:10.1086/284115
Levine JM, Hacker SD, Harley CDG, Bertness MD (1998) Nitrogen effects on an interaction chain in a salt marsh community. Oecologia 117:266–272. doi:10.1007/s004420050657
Lövkvist B (1956) The Cardamine pratensis complex. Outlines of its cytogenetics and taxonomy. PhD dissertation, University of Uppsala, Uppsala
Michalakis Y, Olivieri I, Renaud F, Raymond M (1992) Pleiotropic action of parasites: how to be a good host. Trends Ecol Evol 7:59–62. doi:10.1016/0169-5347(92)90108-N
Morand S, Manning SD, Woolhouse MEJ (1996) Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proc R Soc Lond B 263:119–128. doi:10.1098/rspb.1996.0019
Münzbergová Z (2006) Ploidy level interacts with population size and condition to determine the degree of herbivory damage in plant population. Oikos 115:443–452. doi:10.1111/j.2006.0030-1299.15286.x
Nuismer SL, Cunningham BM (2005) Selection for phenotypic divergence between diploid and autotetraploid Heuchera grossulariifolia. Evolution 59:1928–1935. doi:10.1554/04-715.1
Nuismer SL, Thompson JN (2001) Plant polyploidy and non-uniform effects on insect herbivores. Proc R Soc Lond B 268:1937–1940. doi:10.1098/rspb 2001.1760
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development core team (2013) nlme: Linear and nonlinear mixed effects models. R package version 3.1-108
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. http://www.R-project.org/
Scheines R, Spirtes P, Glymour C, Meek C, Richardson T (1998) The TETRAD project: constraint based aids to causal model specification. Multivar Behav Res 33:65–117. doi:10.1207/s15327906mbr3301_3
Segraves KA, Thompson JN (1999) Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia. Evolution 53:1114–1127. doi:10.2307/2640816
Sharma HC, Venkateswarulu G, Sharma A (2003) Environmental factors influence the expression of resistance to sorghum midge, Stenodiplosis sorghicola. Euphytica 130:365–375
Singer MC, McBride CS (2012) Geographic mosaics of species’ association: a definition and an example driven by plant–insect phenological synchrony. Ecology 93:2658–2673
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
Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst 35:435–466. doi:10.1146/annurev.ecolsys.35.112202.130215
Thomas CD (1984) Oviposition and egg load assessment by Anthocharis cardamines (L.) (Lepidoptera: pieridae). Entomol Gaz 35:145–148
Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago
Thompson JN, Pellmyr O (1992) Mutualism with pollinating seed parasites amid co-pollinators: constraints of specialization. Ecology 73:1780–1791. doi:10.2307/1940029
Thompson JN, Cunningham BM, Segraves KA, Althoff DM, Wagner D (1997) Plant polyploidy and insect/plant interactions. Am Nat 150:730–743. doi:10.1086/286091
Veteli TO, Tegelberg R, Pusenius J, Sipura M, Julkunen-Tiitto R, Aphalo PJ, Tahvanainen J (2003) Interactions between willows and insect herbivores under enhanced ultraviolet-B radiation. Oecologia 137:312–320. doi:10.1007/s00442-003-1298-0
Wiklund C (1984) Egg-laying patterns in butterflies in relation to their phenology and the visual apparency and abundance of their host plants. Oecologia 1:23–29. doi:10.1007/BF00379780
Wiklund C, Åhrberg C (1978) Host plants, nectar source plants, and habitat selection of males and females of Anthocharis cardamines (Lepidoptera). Oikos 31:169–183. doi:10.2307/3543560
Wiklund C, Friberg M (2009) The evolutionary ecology of generalization: among-year variation in host plant use and offspring survival in a butterfly. Ecology 90:3406–3417. doi:10.1890/08-1138.1
Xiang H, Chen J (2004) Interspecific variation of plant traits associated with resistance to herbivory among four species of ficus (Moraceae). Ann Bot 94:377–384. doi:10.1093/aob/mch153
Acknowledgments
Thanks to N. Janz and two anonymous reviewers for comments on the manuscript, and to M. Ahlström, L. Hagström, A. Herrström, J. Oremus and E. Waldén for field assistance. This research was funded by the Swedish Research Council (to J. E.).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Julia Koricheva.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Electronic Supplementary Material.
Online resources Fig. 1. The cage experiment setup.
Rights and permissions
About this article
Cite this article
König, M.A.E., Wiklund, C. & Ehrlén, J. Context-dependent resistance against butterfly herbivory in a polyploid herb. Oecologia 174, 1265–1272 (2014). https://doi.org/10.1007/s00442-013-2831-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-013-2831-4