, Volume 173, Issue 4, pp 1345–1354 | Cite as

Florivore impacts on plant reproductive success and pollinator mortality in an obligate pollination mutualism

  • David M. Althoff
  • Wei Xiao
  • Sarah Sumoski
  • Kari A. Segraves
Plant-microbe-animal interactions - Original research


Florivores are present in many pollination systems and can have direct and indirect effects on both plants and pollinators. Although the impact of florivores are commonly examined in facultative pollination mutualisms, their effects on obligate mutualism remain relatively unstudied. Here, we used experimental manipulations and surveys of naturally occurring plants to assess the effect of florivory on the obligate pollination mutualism between yuccas and yucca moths. Yucca filamentosa (Agavaceae) is pollinated by the moth Tegeticula cassandra (Lepidoptera: Prodoxidae), and the mutualism also attracts two florivores: a generalist, the leaf-footed bug Leptoglossus phyllopus (Hemiptera: Coreidae), and a specialist, the beetle Hymenorus densus (Coleoptera: Tenebrionidae). Experimental manipulations of leaf-footed bug densities on side branches of Y. filamentosa inflorescences demonstrated that feeding causes floral abscission but does not reduce pollen or seed production in the remaining flowers. Similar to the leaf-footed bugs, experimental manipulations of beetle densities within individual flowers demonstrated that beetle feeding also causes floral abscission, but, in addition, the beetles also cause a significant reduction in pollen availability. Path analyses of phenotypic selection based on surveys of naturally occurring plants revealed temporal variation in the plant traits important to plant fitness and the effects of the florivores on fitness. Leaf-footed bugs negatively impacted fitness when fewer plants were flowering and leaf-footed bug density was high, whereas beetles had a positive effect on fitness when there were many plants flowering and their densities were low. This positive effect was likely due to adult beetles consuming yucca moth eggs while having a negligible effect on floral abscission. Together, the actions of both florivores either augmented the relationship of plant traits and fitness or slightly weakened the relationship. Overall, the results suggest that, although florivores are always present during flowering, the impact of florivores on phenotypic selection in yuccas is strongly mitigated by changes in their densities on plants from year to year. In contrast, both florivores consistently influenced pollinator larval mortality through floral abscission, and H. densus beetles additionally via the consumption of pollinator eggs.


Yucca Florivory Leptoglossus Floral abscission Community context 



We thank K. Glennon and A. Moe for helpful comments on the manuscript. T. Starmer provided much appreciated advice on statistics, and M. Deyrup identified the beetle. We are indebted to B. Cunningham for designing and making the insect cages, A. Johncox for assisting with surveys, and M. Sklaney for help with the field work and pollen staining. The Archbold Biological Station provided access to field sites and intellectual support for this study. Funding was provided by the National Science Foundation grant DEB 0743101 to K. Segraves and D. Althoff. The experiments comply with the current laws of the United States of America in which the experiments were performed.


  1. Adler LS (2008) Selection by pollinators and herbivores on attraction and defense. In: Tilmon KJ (ed) Specialization, speciation, and radiation—the evolutionary biology of herbivorous insects. University of California Press, Berkely, pp 162–173Google Scholar
  2. Adler LS, Bronstein JL (2004) Attracting antagonists: does floral nectar increase leaf herbivory? Ecology 85:1519–1526CrossRefGoogle Scholar
  3. Allen RC (1969) A revision of the genus Leptoglossus Guerin (Hemiptera: coreidae). Entomol Am 45:35–140Google Scholar
  4. Althoff D, Segraves K, Sparks J (2004) Characterizing the interaction between the bogus yucca moth and yuccas: do bogus yucca moths impact yucca reproductive success? Oecologia 140:321–327PubMedCrossRefGoogle Scholar
  5. Althoff DM, Segraves KA, Pellmyr O (2005) Community context of an obligate mutualism: pollinator and florivore effects on Yucca filamentosa. Ecology 86:905–913CrossRefGoogle Scholar
  6. Armbruster WS, Lee J, Baldwin BG (2009) Macroevolutionary patterns of defense and pollination in Dalechampia vines: adaptation, exaptation, and evolutionary novelty. Proc Natl Acad Sci USA 106:18085–18090PubMedCrossRefGoogle Scholar
  7. Ashman TL, Penet L (2007) Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gender-dimorphic plant. Am Nat 169:595–608PubMedCrossRefGoogle Scholar
  8. Baranowski RM, Slater JA (1986) Coreidae of Florida (Hemipterea: Heteroptera), vol. 7. Florida Dept of Agricultural and Consumer Services, GainesvilleGoogle Scholar
  9. Botto-Mahan C, Ramírez PA, Gloria Ossa C, Medel R, Ojeda-Camacho M, González AV (2011) Floral herbivory affects female reproductive success and pollinator visitation in the perennial herb Alstroemeria ligtu (Alstroemeriaceae). Int J Plant Sci 172:1130–1136CrossRefGoogle Scholar
  10. Brody AK (1997) Effects of pollinators, herbivores, and seed predators on flowering phenology. Ecology 78:1624–1631CrossRefGoogle Scholar
  11. Bronstein JL, Barbosa P (2002) Multi-trophic/multi-species mutuaistic interactions: the role of non-mutualists in shaping and mediating mutualisms. In: Hawkins BA, Tscharntke T (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 44–65Google Scholar
  12. Bronstein JL, Wilson WG, Morris WF (2003) Ecological dynamics of mutualist/antagonist communities. Am Nat 162:S24–S39PubMedCrossRefGoogle Scholar
  13. Brues CT (1926) Remarkable abundance of a cistelid beetle, with observations on other aggregations of insects. Am Nat 60:526–545CrossRefGoogle Scholar
  14. Campbell DR, Waser NM, Melendez-Ackerman EJ (1997) Analyzing pollinator-mediated selection in a plant hybrid zone: hummingbird visitation patterns on three spatial scales. Am Nat 149:295–345CrossRefGoogle Scholar
  15. Cardel YJ, Koptur S (2010) Effects of florivory on the pollination of flowers: an experimental field study with a perennial plant. Int J Plant Sci 171:283–292CrossRefGoogle Scholar
  16. Cariveau D, Irwin RE, Brody AK, Garcia-Mayeya LS, von der Ohe A (2004) Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits. Oikos 104:15–26CrossRefGoogle Scholar
  17. Caruso CM, Peterson SB, Ridley CE (2003) Natural selection on floral traits of Lobelia (Lobeliaceae): spatial and temporal variation. Am J Bot 90:1333–1340PubMedCrossRefGoogle Scholar
  18. Caruso CM, Scott SL, Wray JC, Walsh CA (2010) Pollinators, herbivores, and the maintenance of flower color variation: a case study with Lobelia siphilitica. Int J Plant Sci 171:1020–1028CrossRefGoogle Scholar
  19. Cascante-Marin A, Wolf JHD, Oostermeijer JGB (2009) Wasp florivory decreases reproductive success in an epiphytic bromeliad. Plant Ecol 203:149–153CrossRefGoogle Scholar
  20. Colautti RI, Barrett SCH (2010) Natural selection and genetic constraints on flowering phenology in an invasive plant. Int J Plant Sci 171:960–971CrossRefGoogle Scholar
  21. Conner JK (1997) Floral evolution in wild radish: the roles of pollinators, natural selection, and genetic correlations among traits. Intern J Plant Sci 158:S108–S120CrossRefGoogle Scholar
  22. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403CrossRefGoogle Scholar
  23. Galen C, Kaczorowski R, Todd SL, Geib J, Raguso RA (2011) Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum. Am Nat 177:258–272PubMedCrossRefGoogle Scholar
  24. Gomez 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
  25. Hanley ME, Lamont BB, Armbruster WS (2009) Pollination and plant defence traits co-vary in Western Australian Hakeas. New Phytol 182:251–260PubMedCrossRefGoogle Scholar
  26. Herrera CM et al (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc Natl Acad Sci USA 99:16823–16828PubMedCrossRefGoogle Scholar
  27. Irwin RE (2000) Hummingbird avoidance of nectar-robbed plants: spatial location or visual cues. Oikos 91:499–506CrossRefGoogle Scholar
  28. Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527CrossRefGoogle Scholar
  29. Irwin RE, Brody AK (2011) Additive effects of herbivory, nectar robbing and seed predation on male and female fitness estimates of the host plant Ipomopsis aggregata. Oecologia 166:681–692PubMedCrossRefGoogle Scholar
  30. Irwin RE, Adler LS, Brody AK (2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85:1503–1511CrossRefGoogle Scholar
  31. Jones EI, Ferriere R, Bronstein JL (2009) Eco-evolutionary dynamics of mutualists and exploiters. Am Nat 174:780–794PubMedCrossRefGoogle Scholar
  32. Kawagoe T, Kudoh H (2010) Escape from floral herbivory by early flowering in Arabidopsis halleri subsp gemmifera. Oecologia 164:713–720PubMedCrossRefGoogle Scholar
  33. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202PubMedCrossRefGoogle Scholar
  34. Kingsolver JG, Schemske DW (1991) Path analyses of selection. Trends Ecol Evol 6:276–280PubMedCrossRefGoogle Scholar
  35. Krupnick GA, Weis AE (1999) The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80:135–149Google Scholar
  36. Lay CR, Linhart YB, Diggle PK (2011) The good, the bad and the flexible: plant interactions with pollinators and herbivores over space and time are moderated by plant compensatory responses. Ann Bot 108:749–763PubMedCrossRefGoogle Scholar
  37. Leavitt H, Robertson IC (2006) Petal herbivory by chrysomelid beetles (Phyllotreta sp.) is detrimental to pollination and seed production in Lepidium papilliferum (Brassicaceae). Ecol Entomol 31:657–660CrossRefGoogle Scholar
  38. Louda SM, Potvin MA (1995) Effect of inflorescence-feeding insects on the demography and lifetime fitness of a native plant. Ecology 76:229–245CrossRefGoogle Scholar
  39. McCall AC (2008) Florivory affects pollinator visitation and female fitness in Nemophila menziesii. Oecologia 155:729–737PubMedCrossRefGoogle Scholar
  40. McCall AC (2010) Does dose-dependent petal damage affect pollen limitation in an annual plant? Bot Bot 88:601–606CrossRefGoogle Scholar
  41. McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365PubMedCrossRefGoogle Scholar
  42. Morris WF, Bronstein JL, Wilson WG (2003) Three-way coexistence in obligate mutualist-exploiter interactions: the potential role of competition. Am Nat 161:860–875PubMedCrossRefGoogle Scholar
  43. Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant–pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40Google Scholar
  44. Oguro M, Sakai S (2009) Floral herbivory at different stages of flower development changes reproduction in Iris gracilipes (Iridaceae). Plant Ecol 202:221–234CrossRefGoogle Scholar
  45. Ornelas JF, González C, Jiménez L, Lara C, Martínez J (2007) Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. II. attracting and rewarding mutualistic and antagonistic visitors. Am J Bot 91:1061–1069CrossRefGoogle Scholar
  46. Parachnowitsch AL, Caruso CM (2008) Predispersal seed herbivores, not pollinators, exert selection on floral traits via female fitness. Ecology 89:1802–1810PubMedCrossRefGoogle Scholar
  47. Parachnowitsch AL, Kessler A (2010) Pollinators exert natural selection on flower size and floral display in Penstemon digitalis. New Phytol 188:393–402PubMedCrossRefGoogle Scholar
  48. Pellmyr O (1992) Evolution of insect pollination and angiosperm diversification. Trends Ecol Evol 7:46–49PubMedCrossRefGoogle Scholar
  49. Pellmyr O (2003) Yuccas, Yucca moths, and coevolution: a review. Ann Missouri Bot Gard 90:35–55CrossRefGoogle Scholar
  50. Pilson D (2000) Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. Oecologia 122:72–82CrossRefGoogle Scholar
  51. Powell J (1992) Interrelationships of yuccas and yucca moths. Trends Ecol Evol 7:10–15PubMedCrossRefGoogle Scholar
  52. Rodriguez-Rodriguez MC, Valido A (2011) Consequences of plant–pollinator and floral-herbivore interactions on the reproductive success of the canary islands endemic Canarina canariensis (Campanulaceae). Am J Bot 98:1465–1474PubMedCrossRefGoogle Scholar
  53. Scheiner SM, Mitchell RJ, Callahan HS (2000) Using path analysis to measure natural selection. J Evol Biol 13:423–433CrossRefGoogle Scholar
  54. Segraves KA (2008) Florivores limit cost of mutualism in the yucca–yucca moth association. Ecology 89:3215–3221CrossRefGoogle Scholar
  55. Sober V, Moora M, Teder T (2010) Florivores decrease pollinator visitation in a self-incompatible plant. Basic Appl Ecol 11:669–675CrossRefGoogle Scholar
  56. Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:S10–S23PubMedCrossRefGoogle Scholar
  57. Strauss SY (1997) Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640–1645CrossRefGoogle Scholar
  58. Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst 35:435–466CrossRefGoogle Scholar
  59. Teixido AL, Mendez M, Valladares F (2011) Flower size and longevity influence florivory in the large-flowered shrub Cistus ladanifer. Acta Oecol Intern J Ecol 37:418–421CrossRefGoogle Scholar
  60. Theis N (2006) Fragrance of canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J Chem Ecol 32:917–927PubMedCrossRefGoogle Scholar
  61. Theis N, Adler L (2011) Advertising to the enemy: Enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93(2):430–435CrossRefGoogle Scholar
  62. Theis N, Lerdau M, Raguso RA (2007) The challenge of attracting pollinators while evading floral herbivores: patterns of fragrance emission in Cirsium arvense and Cirsium repandum (Asteraceae). Int J Plant Sci 168:587–601CrossRefGoogle Scholar
  63. Tsuji K, Sota T (2010) Sexual differences in flower defense and correlated male-biased florivory in a plant-florivore system. Oikos 119:1848–1853CrossRefGoogle Scholar
  64. Weiss MR (1996) Pollen-feeding fly alters floral phenotypic gender in Centropogon solanifolius (Campanulaceae). Biotropica 28:770–773CrossRefGoogle Scholar
  65. Wise MJ, Hebert JB (2010) Herbivores affect natural selection for floral-sex ratio in a field population of horsenettle, Solanum carolinense. Ecology 91:937–943PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • David M. Althoff
    • 1
  • Wei Xiao
    • 2
  • Sarah Sumoski
    • 3
  • Kari A. Segraves
    • 1
  1. 1.Department of BiologySyracuse UniversitySyracuseUSA
  2. 2.Department of Environmental and Forest BiologySUNY-ESFSyracuseUSA
  3. 3.College of William and Mary–Virginia Institute of Marine ScienceGloucester PointUSA

Personalised recommendations