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Environmental context determines within- and potential between-generation consequences of herbivory

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Abstract

Plant tolerance to herbivory may depend on local environmental conditions. Models predict both increased and decreased tolerance with increasing resources. Transgenerational effects of herbivory may result in cross-generation tolerance. We evaluated within- and potential between-generation consequences of deer browsing in light-gap and understory habitats in the forest-edge herb, Campanulastrum americanum. Plants were assigned to deer-browsed, simulated-herbivory, and control (undamaged) treatments in the two light environments. In light gaps, plants were eaten earlier, more frequently, and had less vegetative recovery relative to uneaten plants than in the understory. As a result, browsed light-gap plants had a greater reduction in flowers and fruit than understory plants. This reduced tolerance was in part because deer browsing damaged plants in light gaps more than those in the understory. However, in the simulated herbivory treatment, where damage levels were similar between light habitats, plants growing in high-resource light gaps also had reduced tolerance of herbivory relative to those in the forest understory. C. americanum’s reproductive phenology was delayed by reduced light and the loss of the apical meristem. As a result, deer-browsed plants in the light gap flowered slightly later than uneaten plants in the understory. C. americanum has a polymorphic life history and maternal flowering time influences the frequency of annual and biennial offspring. The later flowering of deer-browsed plants in light gaps will likely result in a reduced frequency of high-fitness annual offspring and an increase in lower fitness biennial offspring. Therefore, additional between-generation costs of herbivory are expected relative to those predicted by fruit number alone.

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References

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

    Article  CAS  PubMed  Google Scholar 

  • Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defences in animals and plants. Nature 401:60–63

    Article  CAS  Google Scholar 

  • Augustine DJ, Frelich LE (1998) Effects of white-tailed deer on populations of understory forb in fragmented deciduous forests. Conserv Biol 12:995–1004

    Article  Google Scholar 

  • Baskin JM, Baskin CC (1984) The ecological life cycle of Campanula americana in northcentral Kentucky. Bull Torrey Bot Club 111:329–337

    Article  Google Scholar 

  • Bergelson J, Crawley MJ (1992) The effects of grazers on the performance of individuals and populations of scarlet-gilia, Ipomopsis aggregata. Oecologia 90:435–444

    Article  Google Scholar 

  • Blundell AG, Peart DR (2001) Growth strategies of a shade tolerant tropical tree: the interactive effects of canopy gaps and simulated herbivory. J Ecol 89:608–615

    Article  Google Scholar 

  • Bullock J, Hill CB, Silvertown J (1994) Demography of Cirsium vulgare in a grazing experiment. J Ecol 82:101–111

    Article  Google Scholar 

  • Cote SD, Rooney TP, Tremblay JP, Dussault C, Waller DM (2004) Ecological impacts of deer overpopulation. Annu Rev Ecol Evol Syst 35:113–147

    Article  Google Scholar 

  • Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol 34:531–564

    Article  Google Scholar 

  • Crawley MJ, Nachapong M (1985) The establishment of seedlings from primary and regrowth seeds of ragwort (Senecio jacobaea). J Ecol 73:255–262

    Article  Google Scholar 

  • Freeman RS, Brody AK, Neefus CD (2003) Flowering phenology and compensation for herbivory in Ipomopsis aggregata. Oecologia 136:394–401

    Article  PubMed  Google Scholar 

  • Galloway LF (2002) The effect of maternal phenology on offspring characters in the herbaceous plant Campanula americana. J Ecol 90:851–858

    Article  Google Scholar 

  • Galloway LF (2005) Maternal effects provide phenotypic adaptation to location environmental conditions. New Phytol 166:93–100

    Article  PubMed  Google Scholar 

  • Galloway LF, Burgess KS (2009) Manipulation of flowering time: phenological integration and maternal effects. Ecology 90:2139–2148

    Article  PubMed  Google Scholar 

  • Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136

    Article  CAS  PubMed  Google Scholar 

  • Galloway LF, Etterson JR (2009) Plasticity to canopy shade in a monocarpic herb: within and between generation effects. New Phytol 182:1003–1012

    Article  Google Scholar 

  • Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. BioScience 53(4):341-356

    Google Scholar 

  • Häsler H, Senn J, Edwards P (2008) Light-dependent growth responses of young Abies alba to simulated ungulate browsing. Funct Ecol 22:48–57

    Google Scholar 

  • Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058

    Article  Google Scholar 

  • Hilbert DW, Swift DM, Detling JK, Dyer MI (1981) Relative growth rates and the grazing optimization hypothesis. Oecologia 51:14–18

    Article  Google Scholar 

  • Holeski LM (2007) Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus. J Evol Biol 20:2092–2100

    Article  CAS  PubMed  Google Scholar 

  • Huhta AP, Rautio P, Hellstrom K, Saari M, Tuomi J (2009) Tolerance of a perennial herb, Pimpinella saxifraga, to simulated flower herbivory and grazing: immediate repair of injury or postponed reproduction? Plant Ecol 201:599–609

    Article  Google Scholar 

  • Husheer SW, Roberston AW, Coomes DA, Frampton CM (2006) Herbivory and plant competition reduce mountain beech seedling growth and establishment in New Zealand. Plant Ecol 183:245–256

    Article  Google Scholar 

  • Irwin DL, Aarssen LW (1996) Effects of nutrient level on cost and benefit of apical dominance in Epilobium ciliatum. Am Midl Nat 136:14–28

    Article  Google Scholar 

  • Kilkenny FF, Galloway LF (2008) Reproductive success in varying light environments: direct and indirect effects of light on plants and pollinators. Oecologia 155:247–255

    Article  PubMed  Google Scholar 

  • Knight TM (2004) The effects of herbivory and pollen limitation on a declining population of Trillium grandiflorum. Ecol Appl 14:915–928

    Article  Google Scholar 

  • Lammerink J, MacGibbon DB, Wallace AR (1984) Effect of the cabbage aphid (Brevicoryne brassicae) on total glucosinolate in the seed of oilseed rape (Brassica napus). N Z J Agric Res 27:89–92

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lennartsson T, Nilsson P, Tuomi J (1998) Induction of overcompensation in the field gentian, Gentianella campestris. Ecology 79:1061–1072

    Google Scholar 

  • Lesage L, Crête M, Huot J, Ouellet JP (2002) Use of forest maps versus field surveys to measure summer habitat selection and sexual segregation in northern white-tailed deer. Can J Zool 80:717–726

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • McGraw JB, Furedi MA (2005) Deer browsing and population viability of a forest understory plant. Science 307:920–922

    Article  CAS  PubMed  Google Scholar 

  • McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40:329–336

    Article  Google Scholar 

  • McShea WJ, Underwood HB, Rappole JH (1997) The science of overabundance: deer ecology and population management. Smithsonian Institution Press, Washington

    Google Scholar 

  • Milbrath LR (2008) Growth and reproduction of invasive Vincetoxicum rossicum and V. nigrum under artificial defoliation and different light environments. Botany 86:1279–1290

    Article  Google Scholar 

  • Mueller RC, Wade BD, Gehring CA, Whitham TG (2005) Chronic herbivory negatively impacts cone and seed production, seed quality and seedling growth of susceptible pinyon pines. Oecologia 143:558–565

    Article  PubMed  Google Scholar 

  • Muth NZ, Kluger EC, Levy JH, Edwards MJ, Niesenbaum RA (2008) Increased per capita herbivory in the shade: necessity, feedback, or luxury consumption? Ecoscience 15:182–188

    Article  Google Scholar 

  • Norghauer JM, Malcolm JR, Zimmerman BL (2008) Canopy cover mediates interactions between a specialist caterpillar and seedlings of a Neotropical tree. J Ecol 96:103–113

    Google Scholar 

  • Nuismer SL, Cunningham BM (2005) Selection for phenotypic divergence between diploid and autotetraploid Heuchera grossulariifolia. Evolution 59:1928–1935

    PubMed  Google Scholar 

  • Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129:407–416

    Article  Google Scholar 

  • Pilson D, Decker KL (2002) Compensation for herbivory in wild sunflower: response to simulated damage by the head-clipping weevil. Ecology 83:3097–3107

    Article  Google Scholar 

  • Rautio P, Huhta AP, Piippo S, Tuomi J, Juenger T, Saari M, Aspi J (2005) Overcompensation and adaptive plasticity of apical dominance in Erysimum strictum (Brassicacae) in response to simulated browsing and resource availability. Oikos 111:179–191

    Article  Google Scholar 

  • Rooney TP, Waller DM (2003) Direct and indirect effects of white-tailed deer in forest ecosystems. For Ecol Manage 181:165–176

    Article  Google Scholar 

  • Russell FL, Zippin SB, Fowler NL (2001) Effects of white-tailed deer (Odocoileus virginianus) on plants, plant populations and communities: a review. Am Midl Nat 146:1–26

    Article  Google Scholar 

  • SAS Institute (2005) SAS/STAT version 9.1.3. SAS Institute, Cary

    Google Scholar 

  • Steets JA, Ashman TL (2004) Herbivory alters the expression of a mixed-mating system. Am J Bot 91:1046–1051

    Article  Google Scholar 

  • Steets JA, Knight TM, Ashman TL (2007) The interactive effects of herbivory and mixed mating for the population dynamics of Impatiens capensis. Am Nat 170:113–127

    Article  PubMed  Google Scholar 

  • Thiemann JA, Webster CR, Jenkins MA, Hurley PM, Rock JH, White PS (2009) Herbaceous-layer impoverishment in a post-agricultural southern Appalachian landscape. Am Midl Nat 162:148–168

    Article  Google Scholar 

  • Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536

    Article  Google Scholar 

  • Tufto J, Andersen R, Linnell J (1996) Habitat use and ecological correlates of home range size in a small cervid: the roe deer. J Anim Ecol 65:715–724

    Article  Google Scholar 

  • Virginia Department of Game and Inland Fisheries (2007) Virginia deer management plan 2006–2015. Wildlife information publication. Virginia Department of Game and Inland Fisheries, Richmond

  • Wallace LL, McNaughton SJ, Coughenour MB (1985) Effects of clipping and four levels of nitrogen on the gas exchange, growth and production of two East African graminiods. Am J Bot 72:222–230

    Article  Google Scholar 

  • Whigham DF (1990) The effect of experimental defoliation on the growth and reproduction of a woodland orchid, Tipularia discolor. Can J Bot 68:1812–1816

    Google Scholar 

  • Wise MJ, Abrahamson WG (2005) Beyond the compensatory continuum: environmental resource levels and plant tolerance of herbivory. Oikos 109:417–428

    Article  Google Scholar 

  • Wise MJ, Abrahamson WG (2007) Effects of resource availability on tolerance of herbivory: a review and assessment of three opposing models. Am Nat 169:443–454

    Article  PubMed  Google Scholar 

  • Wise MJ, Abrahamson WG (2008) Applying the limiting resource model to plant tolerance of apical meristem damage. Am Nat 172:635–647

    Article  PubMed  Google Scholar 

  • Yang LH (2008) Pulses of dead periodical cicadas increase herbivory of American bellflowers. Ecology 89:1497–1502

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Mountain Lake Biological Station (University of Virginia) for logistical support, L. Dierkes and C. Jenkins for field assistance, two anonymous reviewers for comments on an earlier version of the manuscript, and NSF REU-Sites grant DBI-0453380 to M. L. B. S. and DEB-0316298 to L. F. G. for financial support. The experiment complied with the current laws and the authors have no conflict of interest.

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Correspondence to Laura F. Galloway.

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Communicated by Judith Bronstein.

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Lin, S.M., Galloway, L.F. Environmental context determines within- and potential between-generation consequences of herbivory. Oecologia 163, 911–920 (2010). https://doi.org/10.1007/s00442-010-1634-0

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