Skip to main content
SpringerLink
Log in

Feeding damage to plants increases with plant size across 21 Brassicaceae species

  • Plant-microbe-animal interactions - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Plant size is a major predictor of ecological functioning. We tested the hypothesis that feeding damage to plants increases with plant size, as the conspicuousness of large plants makes resource finding and colonisation easier. Further, large plants can be attractive to herbivores, as they offer greater amounts and ranges of resources and niches, but direct evidence from experiments testing size effects on feeding damage and consequently on plant fitness is so far missing. We established a common garden experiment with a plant size gradient (10–130 cm height) using 21 annual Brassicaceae species, and quantified plant size, biomass and number of all aboveground components (flowers, fruits, leaves, stems) and their proportional feeding damage. Plant reproductive fitness was measured using seed number, 1000 seed weight and total seed weight. Feeding damage to the different plant components increased with plant size or component biomass, with mean damage levels being approximately 30 % for flowers, 5 % for fruits and 1 % for leaves and stems. Feeding damage affected plant reproductive fitness depending on feeding damage type, with flower damage having the strongest effect, shown by greatly reduced seed number, 1000 seed weight and total seed weight. Finally, we found an overall negative effect of plant size on 1000 seed weight, but not on seed number and total seed weight. In conclusion, being conspicuous and attractive to herbivores causes greater flower damage leading to higher fitness costs for large plants, which might be partly counterbalanced by benefits such as enhanced competitive/compensatory abilities or more mutualistic pollinator visits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agrawal AA (2001) Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect? Am Nat 157:555–569. doi:10.1086/319932

    Article  CAS  PubMed  Google Scholar 

  • Alford DV, Nilsson C, Ulber B (2003) Insect pests of oilseed rape crops. In: Alford DV (ed) Biocontrol oilseed rape pests. Blackwell, Oxford, pp 9–31

    Chapter  Google Scholar 

  • Alonso C, Herrera CM (1996) Variation in herbivory within and among plants of Daphne laureola (Thymelaeaceae): correlation with plant size and architecture. J Ecol 84:495–502

    Article  Google Scholar 

  • Araujo APA, de D’arc Paula J, Carneiro MAA, Schoereder JH (2006) Effects of host plant architecture on colonization by galling insects. Austral Ecol 31:343–348. doi:10.1111/j.1442-9993.2006.01563.x

    Article  Google Scholar 

  • Barton K (2015) MuMIn: multi-model inference. R package version 1.13.4. http://CRAN.R-project.org/package=MuMIn

  • Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407. doi:10.1086/393620

    Article  CAS  PubMed  Google Scholar 

  • Brown JH, Maurer BA (1986) Body size, ecological dominance and Cope’s rule. Nature 324:248–250

    Article  Google Scholar 

  • Buchanan AL, Underwood N (2013) Attracting pollinators and avoiding herbivores: insects influence plant traits within and across years. Oecologia 173:473–482. doi:10.1007/s00442-013-2629-4

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Castagneyrol B, Giffard B, Péré C, Jactel H (2013) Plant apparency, an overlooked driver of associational resistance to insect herbivory. J Ecol 101:418–429. doi:10.1111/1365-2745.12055

    Article  Google Scholar 

  • Collinge SK, Louda SM (1988) Patterns of resource use by a drosophilid (Diptera) leaf miner on a native crucifer. Ann Entomol Soc Am 81:733–741

    Article  Google Scholar 

  • Dechert G, Ulber B (2004) Interactions between the stem-mining weevils Ceutorhynchus napi Gyll. and Ceutorhynchus pallidactylus (Marsh.) (Coleoptera: Curculionidae) in oilseed rape. Agric For Entomol 6:193–198. doi:10.1111/j.1461-9555.2004.00220.x

    Article  Google Scholar 

  • Donnelly SE, Lortie CJ, Aarssen LW (1998) Pollination in Verbascum thapsus (Scrophulariaceae): the advantage of being tall. Am J Bot 85:1618–1625

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ekbom B, Borg A (1996) Pollen beetle (Meligethes aeneus) oviposition and feeding preference on different host plant species. Entomol Exp Appl 78:291–299. doi:10.1111/j.1570-7458.1996.tb00793.x

    Article  Google Scholar 

  • Endara M-J, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398. doi:10.1111/j.1365-2435.2010.01803.x

    Article  Google Scholar 

  • Espírito-Santo MM, Neves FDS, Andrade-Neto FR, Fernandes GW (2007) Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects. Oecologia 153:353–364. doi:10.1007/s00442-007-0737-8

    Article  PubMed  Google Scholar 

  • Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochem Interact between plants insects. Springer, New York, pp 1–40

    Chapter  Google Scholar 

  • Free JB, Williams IH (1979) The distribution of insect pests on crops of oil-seed rape (Brassica napus L.) and the damage they cause. J Agric Sci 92:139–149

    Article  Google Scholar 

  • Free JB, Ferguson AW, Winfield S (1983) Effect of various levels of infestation by the seed weevil (Ceutorhynchus assimilis Payk.) on the seed yield of oil-seed rape (Brassica napus L.). J Agric Sci 101:589–596

    Article  Google Scholar 

  • Gavloski J, Lamb R (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

    Article  Google Scholar 

  • Giamoustaris A, Mithen R (1996) The effect of flower colour and glucosinolates on the interaction between oilseed rape and pollen beetles. Entomol Exp Appl 80:206–208. doi:10.1111/j.1570-7458.1996.tb00919.x

    Article  CAS  Google Scholar 

  • Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711. doi:10.1111/j.1420-9101.2010.02210.x

    Article  CAS  PubMed  Google Scholar 

  • Hainsworth FR, Wolf LL, Mercier T (1984) Pollination and pre-dispersal seed predation: net effects on reproduction and inflorescence characteristics in Ipomopsis aggregata. Oecologia 63:405–409

    Article  Google Scholar 

  • Haysom KA, Coulson JC (1998) The Lepidoptera fauna associated with Calluna vulgaris: effects of plant architecture on abundance and diversity. Ecol Entomol 23:377–385. doi:10.1046/j.1365-2311.1998.00152.x

    Article  Google Scholar 

  • Heiberger RM (2015) HH: statistical analysis and data display: Heiberger and Holland. R package version 3.1-15. http://CRAN.R-project.org/package=HH

  • Hemptinne J-L, Magro A, Evans EW, Dixon AFG (2012) Body size and the rate of spread of invasive ladybird beetles in North America. Biol Invasions 14:595–605. doi:10.1007/s10530-011-0101-0

    Article  Google Scholar 

  • Herms D, Mattson W (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335. doi:10.1086/417659

    Article  Google Scholar 

  • Juran I, Gothlin Čuljak T, Grubišić D (2011) Rape stem weevil (Ceutorhynchus napi Gyll. 1837) and cabbage stem weevil (Ceutorhynchus pallidactylus Marsh. 1802) (Coleoptera: Curculionidae)—important oilseed rape pests. Agric Conspec Sci 76:93–100

    Google Scholar 

  • Kawano S, Nagai Y (1975) The productive and reproductive biology of flowering plants, 1: life history strategies of three Allium species in Japan. Bot Mag 88:281–318

    Article  Google Scholar 

  • Klotz S, Kühn I, Durka W (2002) BIOLFLOR—Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland (BIOLFLOR database—search and information system on vascular plants in Germany). Schriftenr für Veg 38

  • Lawton JH (1983) Plant architecture and the diversity of phytophagous insects. Annu Rev Entomol 28:23–39

    Article  Google Scholar 

  • Lawton JH, Price PW (1979) Species richness of parasites on hosts: agromyzid flies on the British Umbelliferae. J Anim Ecol 48:619–637

    Article  Google Scholar 

  • McArt SH, Halitschke R, Salminen JP, Thaler JS (2013) Leaf herbivory increases plant fitness via induced resistance to seed predators. Ecology 94:966–975. doi:10.1890/12-1664.1

    Article  Google Scholar 

  • McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365. doi:10.1111/j.1461-0248.2006.00975.x

    Article  PubMed  Google Scholar 

  • Moyes CL, Raybould AF (1997) Herbivory by the cabbage seed weevil (Ceutorhynchus assimilis) in natural populations of Brassica oleracea. Int Symp Brassica 97 Xth Crucif Genet Work 459:315–322

    Google Scholar 

  • Neuvonen S, Niemelä P (1981) Species richness of Macrolepidoptera on Finnish deciduous trees and shrubs. Oecologia 51:364–370

    Article  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. doi: 10.1017/CBO9780511608551

  • Pinheiro J, Bates D, DebRoy S et al (2015) nlme: linear and nonlinear mixed effects models. R package version 3.1-120. http://CRAN.R-project.org/package=nlme%3E

  • Puentes A, Ågren J (2012) Additive and non-additive effects of simulated leaf and inflorescence damage on survival, growth and reproduction of the perennial herb Arabidopsis lyrata. Oecologia 169:1033–1042. doi:10.1007/s00442-012-2276-1

    Article  PubMed  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Remmel T, Tammaru T (2009) Size-dependent predation risk in tree-feeding insects with different colouration strategies: a field experiment. J Anim Ecol 78:973–980. doi:10.1111/j.1365-2656.2009.01566.x

    Article  PubMed  Google Scholar 

  • Reudler Talsma JH, Biere A, Harvey JA, van Nouhuys S (2008) Oviposition cues for a specialist butterfly-plant chemistry and size. J Chem Ecol 34:1202–1212. doi:10.1007/s10886-008-9519-y

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113. doi:10.1111/j.2041-210X.2010.00012.x

    Article  Google Scholar 

  • Schlinkert H (2014) Plant size gradient in Brassicaceae. doi: 10.6084/m9.figshare.1246843

  • Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440. doi:10.1007/s004420050949

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Tenow O, Larsson S (1987) Consumption by needle-eating insects on Scots pine in relation to season and stand age. Ecography (Cop) 10:249–260. doi:10.1111/j.1600-0587.1987.tb00766.x

    Article  Google Scholar 

  • Trumble JT, Kolodny-Hirsch DM, Ting IP (1993) Plant compensation for arthropod herbivory. Annu Rev Entomol 38:93–119

    Article  Google Scholar 

  • Ulber B (2003) Parasitoids of Ceutorhynchid stem weevils. In: Alford DV (ed) Biocontrol oilseed rape pests. Blackwell, Oxford, pp 87–96

    Chapter  Google Scholar 

  • Vasconcellos-Neto J, Ferreira Monteiro R (1993) Inspection and evaluation of host plant by the butterfly Mechanitis lysimnia (Nymph., Ithomiinae) before laying eggs: a mechanism to reduce intraspecific competition. Oecologia 95:431–438. doi:10.1007/BF00320999

    Article  Google Scholar 

  • Weiner J (1985) Size hierarchies in experimental populations of annual plants. Ecology 66:743–752. doi:10.2307/1940535

    Article  Google Scholar 

  • Williams IH (2010) The major insect pests of oilseed rape in Europe and their management: an overview. In: Williams IH (ed) Biocontrol-based Integr Manag oilseed rape pests. Springer, Dordrecht, pp 1–44

    Chapter  Google Scholar 

  • Williams IH, Free JB (1978) The feeding and mating behaviour of pollen beetles (Meligethes aeneus Fab.) and seed weevils (Ceutorhynchus assimilis Payk.) on oil-seed rape (Brassica napus L.). J Agric Sci 91:453–459. doi:10.1017/S0021859600046554

    Article  Google Scholar 

  • Williams IH, Free JB (1979) Compensation of oil-seed rape (Brassica napus L.) plants after damage to their buds and pods. J Agric Sci 92:53–59. doi:10.1017/S0021859600060494

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. doi:10.1111/j.2041-210X.2009.00001.x

    Article  Google Scholar 

Download references

Acknowledgments

Special thanks for help in the field go to Susanne Jahn and Brigitte Jünemann, as well as to Christiane Schlinkert, Eugen Schlinkert, Barbara Scheid, Christina Fischer, Verena Rösch, Georg Everwand, Jenny Osterburg, Annabelle Rohlfing, Anna-Katharina Franke, Petra Kubisch, Alexandra Arndt, Carina Burmeister and Felix Steinmeyer. KWS SAAT and the botanical gardens of the universities of Bayreuth and Göttingen provided part of the seeds. We thank Carsten Thies for advice and Kristy Udy for linguistic improvements of the manuscript and two anonymous reviewers for their comments and suggestions, which improved the manuscript. H.S. was supported by the Ministry of Science and Culture of Lower Saxony.

Author information

Authors and Affiliations

  1. Agroecology, Georg-August-University, Grisebachstraße 6, 37077, Göttingen, Germany

    Hella Schlinkert, Catrin Westphal, Yann Clough, Martin Ludwig & Teja Tscharntke

  2. Centre for Environmental and Climate Research, Sölvegatan 37, 223 62, Lund, Sweden

    Yann Clough

  3. Department Phytomedicine, Institute of Horticultural Production Systems, Leibniz University Hannover, Herrenhäuserstr. 2, 30419, Hannover, Germany

    Martin Ludwig

  4. Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB, Wageningen, The Netherlands

    Patrick Kabouw

Authors
  1. Hella Schlinkert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catrin Westphal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yann Clough
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martin Ludwig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patrick Kabouw
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Teja Tscharntke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hella Schlinkert.

Additional information

Communicated by Andreas Prinzing.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schlinkert, H., Westphal, C., Clough, Y. et al. Feeding damage to plants increases with plant size across 21 Brassicaceae species. Oecologia 179, 455–466 (2015). https://doi.org/10.1007/s00442-015-3353-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3353-z

Keywords

Search

Navigation