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Oecologia

, Volume 166, Issue 3, pp 681–692 | Cite as

Additive effects of herbivory, nectar robbing and seed predation on male and female fitness estimates of the host plant Ipomopsis aggregata

  • Rebecca E. Irwin
  • Alison K. Brody
Plant-Animal interactions - Original Paper

Abstract

Many antagonistic species attack plants and consume specific plant parts. Understanding how these antagonists affect plant fitness individually and in combination is an important research focus in ecology and evolution. We examined the individual and combined effects of herbivory, nectar robbing, and pre-dispersal seed predation on male and female estimates of fitness in the host plant Ipomopsis aggregata. By examining the effects of antagonists on plant traits, we were able to tease apart the direct consumptive effects of antagonists versus the indirect effects mediated through changes in traits important to pollination. In a three-way factorial field experiment, we manipulated herbivory, nectar robbing, and seed predation. Herbivory and seed predation reduced some male and female fitness estimates, whereas plants tolerated the effects of robbing. The effects of herbivory, robbing, and seed predation were primarily additive, and we found little evidence for non-additive effects of multiple antagonists on plant reproduction. Herbivory affected plant reproduction through both direct consumptive effects and indirectly through changes in traits important to pollination (i.e., nectar and phenological traits). Conversely, seed predators primarily had direct consumptive effects on plants. Our results suggest that the effects of multiple antagonists on estimates of plant fitness can be additive, and investigating which traits respond to damage can provide insight into how antagonists shape plant performance.

Keywords

Herbivory Ipomopsis aggregata Nectar robbing Nectar Phenology Pollination Pollen deposition Seed predation Trait-based approach 

Notes

Acknowledgments

We thank L. Burkle, B. Degasparis, E. Deliso, K. Fitzgerald, E. Henry, A. Rastogi, K. Ritter, and A. Schuett for help in the field and lab. R. Rosetti from the Dartmouth Women in Science Program helped count pollen for the male function estimates. A. Carper, G. Clarke, J. Evans, Z. Gezon, N. Gotelli, E. Hart, J. Manson, C. Orians, R. Petipas, R. Schaeffer, and two anonymous reviewers provided valuable comments on the manuscript. Field and lab work were funded by the National Science Foundation (NSF) DEB-9806501, and supplies and lab assistance for pollen counting were provided by NSF DEB-0455348 and the Dartmouth Women in Science Program.

References

  1. Adler LS, Karban R, Strauss SY (2001) Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecology 82:2032–2044CrossRefGoogle Scholar
  2. Ashman T-L (1998) Is relative pollen production or removal a good predictor of relative male fitness? An experimental exploration with wild strawberry (Fragaria virginiana, Rosaceae). Am J Bot 85:1166–1171CrossRefGoogle Scholar
  3. Bergelson J, Crawley MJ (1992) Herbivory and Ipomopsis aggregata: the disadvantages of being eaten. Am Nat 139:870–882CrossRefGoogle Scholar
  4. Brody AK (1991) Pre-dispersal seed predation by Hylemya (Delia) sp. (Diptera: Anthomyiidae): mechanisms and consequences of oviposition choice (Ph.D. thesis). University of California, DavisGoogle Scholar
  5. Brody AK (1992) Oviposition choices by a predispersal seed predator (Hylemya sp.). 1. Correspondence with hummingbird pollinators, and the role of plant size, density and floral morphology. Oecologia 91:56–62Google Scholar
  6. Brody AK, Mitchell RJ (1997) Effects of experimental manipulation of inflorescence size on pollination and pre-dispersal seed predation in the hummingbird-pollinated plant Ipomopsis aggregata. Oecologia 110:86–93CrossRefGoogle Scholar
  7. Brody AK, Waser NM (1995) Oviposition patterns and larval success of a pre-dispersal seed predator attacking two confamilial host plants. Oikos 74:447–452CrossRefGoogle Scholar
  8. Brody AK, Irwin RE, McCutcheon ML, Parsons EC (2008) Interactions between nectar robbers and seed predators mediated by a shared host plant, Ipomopsis aggregata. Oecologia 155:75–84PubMedCrossRefGoogle Scholar
  9. Burkle LA, Irwin RE, Newman DA (2007) Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant life-history traits. Am J Bot 94:1935–1943PubMedCrossRefGoogle Scholar
  10. Campbell DR, Halama KJ (1993) Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74:1043–1051CrossRefGoogle Scholar
  11. Collett D (2003) Modelling binary data, 2nd edn. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  12. Crawley MJ (1983) Herbivory: the dynamics of animal–plant interactions. Blackwell Scientific, OxfordGoogle Scholar
  13. Crawley MJ (1997) Plant–herbivore dynamics. In: Crawley MJ (ed) Plant ecology. Blackwell, Oxford, pp 401–474Google Scholar
  14. Danckwerts JE (1993) Reserve carbon and photosynthesis: their role in regrowth of Themeda triandra, a widely distributed subtropical graminaceous species. Funct Ecol 7:634–641CrossRefGoogle Scholar
  15. Engel EC, Irwin RE (2003) Linking pollinator-visitation rate and pollen receipt. Am J Bot 90:1612–1618CrossRefGoogle Scholar
  16. Freeman RS, Brody AK, Neefus CD (2003) Flowering phenology and compensation for herbivory in Ipomopsis aggregata. Oecologia 136:394–401PubMedCrossRefGoogle Scholar
  17. Gómez JM (2003) Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. Am Nat 162:242–256PubMedCrossRefGoogle Scholar
  18. Gómez JM, Perfectti F, Bosch J, Camacho JPM (2009) A geographic selection mosaic in a generalized plant–pollinator–herbivore system. Ecol Monogr 79:245–263CrossRefGoogle Scholar
  19. Gronemeyer PA, Dilger BJ, Bouzat JL, Paige KN (1997) The effects of herbivory on paternal fitness in scarlet gilia: better moms also make better pops. Am Nat 150:592–602PubMedCrossRefGoogle Scholar
  20. Houle G, Simard G (1996) Additive effects of genotype, nutrient availability and type of tissue damage on the compensatory response of Salix planifolia spp. planifolia to stimulated herbivory. Oecologia 107:373–378CrossRefGoogle Scholar
  21. Hufbauer RA, Root RB (2002) Interactive effects of different types of herbivore damage: Trirhabda beetle larva and Philaenus spittlebugs on goldenrod (Solidago altissima). Am Midl Nat 147:204–213CrossRefGoogle Scholar
  22. Irwin RE (2006) Consequences of direct versus indirect species interactions to selection on traits: pollination and nectar robbing in Ipomopsis aggregata. Am Nat 167:315–328PubMedCrossRefGoogle Scholar
  23. Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527CrossRefGoogle Scholar
  24. Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80:1703–1712Google Scholar
  25. Irwin RE, Brody AK (2000) Consequences of nectar robbing for realized male function in a hummingbird-pollinated plant. Ecology 81:2637–2643CrossRefGoogle Scholar
  26. Irwin RE, Brody AK, Waser NM (2001) The impact of floral larceny on individuals, populations, and communities. Oecologia 129:161–168CrossRefGoogle Scholar
  27. Irwin RE, Adler LS, Brody AK (2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85:1503–1511CrossRefGoogle Scholar
  28. Irwin RE, Galen C, Rabenold JJ, Kaczorowski R, McCutcheon ML (2008) Mechanisms of tolerance to floral larceny in two animal-pollinated wildflowers, Polemonium viscosum and Ipomopsis aggregata. Ecology 89:3093–3104CrossRefGoogle Scholar
  29. Juenger T, Bergelson J (1997) Pollen and resource limitation of compensation to herbivory in scarlet gilia, Ipomopsis aggregata. Ecology 78:1684–1695Google Scholar
  30. Juenger T, Bergelson J (1998) Pairwise versus diffuse natural selection and the multiple herbivores of scarlet gilia, Ipomopsis aggregata. Evolution 52:1583–1592CrossRefGoogle Scholar
  31. 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 54:764–777PubMedGoogle Scholar
  32. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
  33. Kolb A, Ehrlén J, Eriksson O (2007) Ecological and evolutionary consequences of spatial and temporal variation in pre-dispersal seed predation. Perspect Plant Ecol Evol Syst 9:79–100CrossRefGoogle Scholar
  34. Maron JL (1998) Insect herbivory above- and belowground: individual and joint effects on plant fitness. Ecology 79:1281–1293CrossRefGoogle Scholar
  35. Marquis RJ (1992) The selective impact of herbivores. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens. University of Chicago Press, Chicago, pp 301–325Google Scholar
  36. Mitchell RJ (1993) Adaptive significance of Ipomopsis aggregata nectar production—observation and experiment in the field. Evolution 47:25–35CrossRefGoogle Scholar
  37. Mitchell RJ, Waser NM (1992) Adaptive significance of Ipomopsis aggregata nectar production: pollination success of single flowers. Ecology 73:633–638CrossRefGoogle Scholar
  38. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405CrossRefGoogle Scholar
  39. Morris WF et al (2007) Direct and indirect interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029PubMedCrossRefGoogle Scholar
  40. Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40Google Scholar
  41. Paige KN (1992) Overcompensation in response to mammalian herbivory: from mutualistic to antagonistic interactions. Ecology 73:2076–2085CrossRefGoogle Scholar
  42. Paige KN, Whitham TG (1987) Overcompensation in response to herbivory: the advantage of being eaten. Am Nat 129:407–416CrossRefGoogle Scholar
  43. Petraitis PS, Dunham AE, Niewiarowski PH (1996) Inferring multiple causality: the limitations of path analysis. Funct Ecol 10:421–431CrossRefGoogle Scholar
  44. Pleasants JM (1983) Nectar production in Ipomopsis aggregata (Polemoniaceae). Am J Bot 70:1468–1475CrossRefGoogle Scholar
  45. Scheiner SM (1993) MANOVA: multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New YorkGoogle Scholar
  46. Sharaf KE, Price MV (2004) Does pollination limit tolerance to browsing in Ipomopsis aggregata? Oecologia 138:396–404PubMedCrossRefGoogle Scholar
  47. Stanton ML, Ashman TL, Galloway LF, Young HJ (1992) Estimating male fitness of plants in natural populations. In: Wyatt R (ed) Ecology and evolution of plant reproduction: new approaches. Chapman & Hall, New York, pp 62–90Google Scholar
  48. Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol Syst 35:435–466CrossRefGoogle Scholar
  49. Strauss SY, Conner JK, Rush SL (1996) Foliar herbivory affects floral characters and plant attractiveness to pollinators: implications for male and female plant fitness. Am Nat 147:1098–1107CrossRefGoogle Scholar
  50. Strauss SY, Sahli H, Conner JK (2005) Toward a more trait-centered approach to diffuse (co)evolution. New Phytol 165:81–90PubMedCrossRefGoogle Scholar
  51. Suarez LH, Gonzalez WL, Gianoli E (2009) Foliar damage modifies floral attractiveness to pollinators in Alstroemeria exerens. Evol Ecol 23:545–555CrossRefGoogle Scholar
  52. Torres I, Salinas L, Lara C, Castillo-Guevara C (2008) Antagonists and their effects in a hummingbird–plant interaction: field experiments. Ecoscience 15:65–72Google Scholar
  53. Waser NM (1978) Competition for hummingbird pollination and sequential flowering in Colorado wildflowers. Ecology 59:934–944CrossRefGoogle Scholar
  54. Waser NM, Price MV (1989) Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43:1097–1109CrossRefGoogle Scholar
  55. Waser NM, Price MV (1991) Reproductive costs of self-pollination in Ipomopsis aggregata: are ovules usurped? Am J Bot 78:1036–1043CrossRefGoogle Scholar
  56. Wolf PG, Campbell DR (1995) Hierarchical analysis of allozymic and morphometric variation in a montane herb, Ipomopsis aggregata (Polemoniaceae). J Hered 86:386–394Google Scholar
  57. Wootton JT (1993) Indirect effects and habitat use in an intertidal community: interaction chains and interaction modifications. Am Nat 141:71–89CrossRefGoogle Scholar
  58. Zhang Y-W, Zhao QYJ-M, Guo Y-H (2009) Differential effects of nectar robbing by the same bumble-bee species on three sympatric Corydalis species with varied mating systems. Ann Bot 104:33–39PubMedCrossRefGoogle Scholar
  59. Zimmerman M (1980) Reproduction in Polemonium: pre-dispersal seed predation. Ecology 61:502–506CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of BiologyDartmouth CollegeHanoverUSA
  2. 2.Rocky Mountain Biological LabCrested ButteUSA
  3. 3.Department of BiologyUniversity of VermontBurlingtonUSA

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