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Does pollination limit tolerance to browsing in Ipomopsis aggregata?

  • Plant Animal Interactions
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Abstract

Ungulate browsing of flowering stalks of the semelparous herb Ipomopsis aggregata leads to regrowth of lateral inflorescences, a response that has been reported to yield overcompensation in some cases (browsed plants with higher reproductive success than unbrowsed), but undercompensation in others. Little is known about the mechanisms that cause such variable tolerance to herbivory. We explored one possible mechanism—variation in effects of browsing on pollination—by clipping I. aggregata inflorescences to mimic browsing, observing subsequent visits by pollinators and nectar-robbers, and adding pollen by hand to flowers of some clipped and unclipped plants. Clipping reduced floral display size and increased inflorescence branching, but neither hummingbirds, the primary pollinators, nor nectar-robbing bumblebees showed any preference for unclipped versus clipped plants. Clipping delayed flowering; this shift in phenology caused clipped plants to miss the peak of hummingbird activity and to have lower per-flower visitation rates than unclipped controls in one year, but to have greater overlap with birds and higher visitation rates in the subsequent year. In three sites and 2 years, clipped plants exposed to natural pollination suffered extreme undercompensation, producing on average only 16% as many seeds as unclipped controls. This was not directly attributable to clipping effects on pollination, however, because clipped plants were unable to increase fecundity when provided with supplemental pollen by hand. Taken altogether, our results suggest that compensation was constrained less by indirect effects of browsing on pollination than by its direct impacts on resource availability and hence on the ability of plants to regrow lost inflorescence tissue and to fill seeds. Exploring the physiological and developmental processes involved in regrowth of inflorescences and provisioning of seeds is a promising future direction for research designed to understand variation in browsing tolerance.

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References

  • Anderson LL, Paige KN (2003) Multiple herbivores and coevolutionary interactions in an Ipomopsis hybrid swarm. Evol Ecol 17:139–156

    Article  Google Scholar 

  • Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. Am Nat 127:870–892

    Article  Google Scholar 

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

    Google Scholar 

  • Bergelson J, Crawley MJ (1992b) Herbivory and Ipomopsis aggregata: the disadvantages of being eaten. Am Nat 139:870–882

    Article  Google Scholar 

  • Brody AK (1992) Oviposition choices by a predispersal seed predator (Hylemya sp.): correspondence with hummingbird pollinators, and the role of plant size, density and floral morphology. Oecologia 91:56–62

    Google Scholar 

  • Brody AK (1997) Effects of pollinators, herbivores, and seed predators on flowering phenology. Ecology 78:1624–1631

    Google Scholar 

  • 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 110:86–93

    Article  Google Scholar 

  • Brody AK, Morita SI (2000) A positive association between oviposition and fruit set: female choice or manipulation? Oecologia 124:418–425

    Google Scholar 

  • Cabin RJ, Mitchell RJ (2002) To Bonferroni or not to Bonferroni: when and how are the questions. Bull Ecol Soc Am 81:246–248

    Google Scholar 

  • Calder WA (1987) Southbound through Colorado: migration of rufous hummingbirds. Natl Geogr Res 3:40–51

    Google Scholar 

  • Calder WA (1991) Territorial hummingbirds. Natl Geogr Res 7:56–69

    Google Scholar 

  • Campbell DR (1991) Effects of floral traits on sequential components of fitness in Ipomopsis aggregata. Am Nat 137:713–737

    Article  Google Scholar 

  • Campbell DR, Halama KJ (1993) Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74:1043–1051

    Google Scholar 

  • Campbell DR, Waser NM, Price MV, Lynch EA, Mitchell RJ (1991) Components of phenotypic selection: pollen export and flower corolla width in Ipomopsis aggregata. Evolution 45:1458–1467

    Google Scholar 

  • De Jong TJ, Waser NM, Price MV, Ring RM (1992) Plant size, geitonogamy, and seed set in Ipomopsis aggregata. Oecologia 89:310–315

    Google Scholar 

  • Elam DR, Linhart YD (1988) Pollination and seed production in Ipomopsis aggregata: differences among and within flower color morphs. Am J Bot 75:1262–1274

    Google Scholar 

  • Freeman RS, Neefus CD, Brody AK (2003) The effects of elevation and herbivory on the reproductive success of Ipomopsis aggregata (Polemoniaceae). Oecologia (in press)

  • 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 150:592–602

    Article  Google Scholar 

  • Hainsworth FR, Wolf LL, Mercier T (1985) Pollen limitation in a monocarpic species, Ipomopsis aggregata. J Ecol 73:263–270

    Google Scholar 

  • Irwin RE, Brody AK (1999) Nectar-robbing bumblebees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80:1703–1712

    Google Scholar 

  • Juenger T, Bergelson J (1997) Pollen and resource limitation of compensation to herbivory in scarlet gilia, Ipomopsis aggregata. Ecology 78:1684–1695

    Google Scholar 

  • Juenger T, Bergelson J (1998) Pairwise versus diffuse natural selection and the multiple herbivores of scarlet gilia, Ipomopsis aggregata. Evolution 52:1583–1592

    Google Scholar 

  • Juenger T, Bergelson J (2000a) Does early season browsing influence the effect of self-pollination in scarlet gilia? Ecology 81:41–48

    Google Scholar 

  • Juenger T, Bergelson J (2000b)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

    CAS  PubMed  Google Scholar 

  • Krupnick GA, Weis AE (1999) The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80:135–149

    Google Scholar 

  • Krupnick GA, Weis AE, Campbell DR (1999) The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80:125–134

    Google Scholar 

  • Lehtila K, Strauss SY (1997) Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphanistrum. Oecologia 111:396–403

    Article  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  Google Scholar 

  • Marquis RJ (1992) Selective impact of herbivores. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 301–325

  • 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 

  • Mayfield MM, Waser NM, Price MV (2001) Exploring the “most effective pollinator principle” with complex flowers: bumblebees and Ipomopsis aggregata. Ann Bot 88:591–596

    Article  Google Scholar 

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

    Google Scholar 

  • Mitchell RJ (1994) Effects of floral traits, pollinator visitation, and plant size on Ipomopsis aggregata fruit production. Am Nat 143:871–889

    Article  Google Scholar 

  • Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40

    Google Scholar 

  • Paige KN (1994) Herbivory and Ipomopsis aggregata: differences in response, differences in experimental protocol: a reply to Bergelson and Crawley. Am Nat 143:739–749

    Article  Google Scholar 

  • Paige KN (1999) Regrowth following ungulate herbivory in Ipomopsis aggregata: geographic evidence for overcompensation. Oecologia 118:316–323

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Paige KN, Williams B, Hickox T (2001) Overcompensation through the paternal component of fitness in Ipomopsis arizonica. Oecologia 128:72–76

    Article  Google Scholar 

  • Price MV, Waser NM (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79:1261–1271

    Google Scholar 

  • Santandreu M, Lloret F (1999) Effect of flowering phenology and habitat on pollen limitation in Erica multiflora. Can J Bot 77:734–743

    Article  Google Scholar 

  • SAS (2000) JMP statistics and graphics guide. SAS Institute, Cary, N.C.

  • Schultz JC (2002) How plants fight dirty. Nature 416:267

    Article  CAS  PubMed  Google Scholar 

  • Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595

    Google Scholar 

  • Strauss SY (1997) Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640–1645

    Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    PubMed  Google Scholar 

  • 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 147:1098–1107

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Tilman D (1987) The importance of the mechanisms of interspecific competition. Am Nat 129:769–774

    Article  Google Scholar 

  • Vail SG (1992) Selection for overcompensatory plant responses to herbivory: a mechanism for the evolution of plant-herbivore mutualism. Am Nat 139:1–8

    Article  Google Scholar 

  • Waser NM (1976) Food supply and nest timing of broad-tailed hummingbirds in the Rocky Mountains. Condor 78:133–135

    Google Scholar 

  • Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two co-occurring wildflowers. Ecology 59:934–944

    Google Scholar 

  • Waser NM (1979) Pollinator availability as a determinant of flowering time in ocotillo (Fouquieria splendens). Oecologia 39:107–121

    Google Scholar 

  • Waser NM, Price MV (1989) Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43:1097–1109

    Google Scholar 

  • Waser NM, Price MV (1991) Reproductive costs of self-pollination in Ipomopsis aggregata: are ovules usurped? Am J Bot 78:1036–1043

    Google Scholar 

  • Waser NM, Price MV, Shaw RG (2000) Outbreeding depression varies among cohorts of Ipomopsis aggregata planted in nature. Evolution 54:485–491

    CAS  PubMed  Google Scholar 

  • Whitham TG, Maschinski J, Larson KC, Paige KN (1991) Plant responses to herbivory: the continuum from negative to positive and underlying physiological mechanisms. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 227–256

  • Wolf LL, Hainsworth FR (1991) Hummingbird foraging patterns: visits to clumps of Ipomopsis aggregata inflorescences. Anim Behav 41:803–812

    Google Scholar 

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Acknowledgements

Thanks to Nick Waser, Becky Irwin, Alison Brody, Diane Campbell, Amity Wilczek, Brian Farrell, Ken Paige, and an anonymous referee for advice and editorial help; to Ben Koch, Elliot Wilkinson, and Twila Patterson for field assistance; and to B. Barr for snowmelt and precipitation data. This work was supported by awards to K.S. from the NSF Research Experience for Undergraduates program (DBI-9987953), the Harvard College Research Program, and the Garden Club of America Clara Carter Higgins Scholarship; and from NSF grant DEB-9805034 to M.P.

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  1. Katherine E. Sharaf

    Present address: National Environmental Trust, 1200 18th Street NW, Suite 500, Washington, DC 20036, USA

Authors and Affiliations

  1. Department of Biology, Harvard University, Cambridge, MA 02138, USA

    Katherine E. Sharaf

  2. Department of Biology, University of California, Riverside, CA 92521, USA

    Mary V. Price

  3. Rocky Mountain Biological Laboratory, P.O.B. 519, Crested Butte, CO 81224, USA

    Katherine E. Sharaf & Mary V. Price

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  1. Katherine E. Sharaf
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Correspondence to Mary V. Price.

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Sharaf, K.E., Price, M.V. Does pollination limit tolerance to browsing in Ipomopsis aggregata?. Oecologia 138, 396–404 (2004). https://doi.org/10.1007/s00442-003-1436-8

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