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Flowering phenology and female fitness: impact of a pre-dispersal seed predator on a sexually polymorphic species

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In order to produce seeds, animal-pollinated plants must flower synchronously with and be attractive to their pollinators while avoiding antagonists. Here, we explore temporal and inter-individual patterns in pollination and pre-dispersal seed predation of Dianthus sylvestris by Hadena moths, within and among three sex morphs. We scored plants that started flowering at different periods in 2001 and 2003 and found that fruit set decreased and predation rates increased over one season, and most of the other season, granting a female reproductive advantage to early flowering plants, though, we found no morph-specific temporal patterns. Female plants set more fruits, and more of their fruits escaped predation in one year, but this did not grant them a reproductive advantage since they produce fewer flowers per plant than the other morphs. Instead, mixed plants showed a clear female reproductive advantage. We also examined predation types by Hadena and seed production in attacked and intact fruits of individually marked flowers. Though female Hadena moths laid eggs preferentially into perfect flowers, flower sexes suffered similar predation by itinerant caterpillars. Attacked fruits contained fewer and lighter seeds than un-attacked ones. We conclude that pre-dispersal seed predation by Hadena may select on flowering onset of this sexually polymorphic species.

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  1. Adler LS, Bronstein JL (2004) Attracting antagonists: does floral nectar increase leaf herbivory? Ecology 85:1519–1526. doi:10.1890/03-0409

  2. Alonso C (2003) Herbivores do not discriminate between leaves of female and hermaphrodite individuals of gynodioecious Daphne laureola (Thymelaeaceae). Oikos 101:505–510. doi:10.1034/j.1600-0706.2003.12115.x

  3. Ashman T-L (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81:2577–2591

  4. Ashman T-L (2002) The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology 83:1175–1184

  5. Ashman T-L (2006) The evolution of separate sexes: a focus on the ecological context. In: Barrett SCH, Harder LD (eds) The ecology and evolution of flowers. Oxford University Press, Oxford, UK, pp 419–465

  6. Ashman T-L, Penet L (2007) Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gynodioecious plant. Am Nat 169:595–608. doi:10.1086/513150

  7. Ashman T-L, Stanton M (1991) Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72:993–1003. doi:10.2307/1940599

  8. Ashman T-L, Cole DH, Bradburn M (2004) Sex-differential resistance and tolerance to herbivory in a gynodioecious wild strawberry. Ecology 85:2550–2559. doi:10.1890/03-0495

  9. Asikainen E, Mutikainen P (2005) Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum. Ann Bot (Lond) 95:879–886. doi:10.1093/aob/mci094

  10. Augspurger CK (1981) Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62:775–788. doi:10.2307/1937745

  11. Baker HG (1948) Corolla-size in gynodioecious and gynomonoecious species of flowering plants. Proc Leeds Philos Lit Soc Sci 5:136–139

  12. Biere A, Honders SJ (1996) Impact of flowering phenology of Silene alba and S. dioica on susceptibility to fungal infection and seed predation. Oikos 77:467–480. doi:10.2307/3545936

  13. Biere A, Elzinga JA, Honders SC, Harvey JA (2002) A plant pathogen reduces the enemy-free space of an insect herbivore on a shared host plant. Proc R Soc Lond B Biol Sci 269:2197–2204. doi:10.1098/rspb.2002.2147

  14. Bopp S, Gottsberger G (2004) Importance of Silene latifolia ssp. alba and S. dioica (Caryophyllaceae) as host plants of the parasitic pollinator Hadena bicruris (Lepidoptera, Noctuidae). Oikos 105:221–228. doi:10.1111/j.0030-1299.2004.12625.x

  15. Brody AK (1992) Oviposition choices by a pre-dispersal seed predator (Hylemya sp.). I. Correspondence with hummingbird pollinators, and the role of plant size, density and floral morphology. Oecologia 91:56–62

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

  17. 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. doi:10.1007/s004420050136

  18. 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 104:15–26. doi:10.1111/j.0030-1299.2004.12641.x

  19. Collin CL, Shykoff JA (2003) Outcrossing rates in the gynomonoecious-gynodioecious species Dianthus sylvestris Wulf. (Caryophyllaceae). Am J Bot 90:549–585. doi:10.3732/ajb.90.4.579

  20. Collin CL, Pennings PS, Rueffler C, Widmer A, Shykoff JA (2002) Natural enemies and sex: how seed predators and pathogens contribute to sex-differential reproductive success in a gynodioecious plant. Oecologia 131:94–102. doi:10.1007/s00442-001-0854-8

  21. de Jong TJ, Waser NM, Klinkhamer PGL (1993) Geitonogamy: the neglected side of selfing. Trends Ecol Evol 8:321–325. doi:10.1016/0169-5347(93)90239-L

  22. Dufaÿ M, Anstett M-C (2003) Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100:3–14. doi:10.1034/j.1600-0706.2003.12053.x

  23. Eckhart VM (1992) The genetics of gender and the effects of gender on floral characters in gynodioecious Phacelia linearis (Hydrophyllaceae). Am J Bot 79:792–800. doi:10.2307/2444946

  24. Ehlers BK, Thompson JD (2004) Temporal variation in sex allocation in hermaphrodites of gynodioecious Thymus vulgaris L. J Ecol 92:15–23. doi:10.1111/j.1365-2745.2004.00846.x

  25. Ehrlén J, Käck S, Ågren J (2002) Pollen limitation, seed predation and scape length in Primula farinosa. Oikos 97:45–51. doi:10.1034/j.1600-0706.2002.970104.x

  26. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439. doi:10.1016/j.tree.2007.05.006

  27. English-Loeb GM, Karban R (1992) Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae). Oecologia 89:588–595

  28. Erhardt A (1988) Pollination and reproduction in Dianthus silvester Wulf. In: Cresti M, Gori P, Pacini E (eds) Sexual reproduction in higher plants. Springer, Berlin, pp 351–356

  29. Fenner M, Cresswell JE, Hurley RA, Baldwin T (2002) Relationship between capitulum size and pre-dispersal seed predation by insect larvae in common Asteraceae. Oecologia 130:72–77

  30. Galen C (1999a) Why do flowers vary? Bioscience 49:631–640. doi:10.2307/1313439

  31. Galen C (1999b) Flowers and enemies: predation by nectar-thieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos 85:426–434. doi:10.2307/3546692

  32. Giles BE, Pettersson TM, Carlsson-Granér U, Ingvarsson PK (2006) Natural selection on floral traits of female Silene dioica by a sexually transmitted disease. New Phytol 169:729–739. doi:10.1111/j.1469-8137.2005.01544.x

  33. Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515. doi:10.1038/373512a0

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

  35. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492. doi:10.1146/annurev.es.02.110171.002341

  36. Kephart S, Reynolds RJ, Rutter MT, Fenster CB, Dudash MR (2006) Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms. New Phytol 169:667–680. doi:10.1111/j.1469-8137.2005.01619.x

  37. Kesseli R, Jain SK (1984) An ecological genetics study in Limnanthes douglasii (Limnanthaceae). Am J Bot 71:775–786. doi:10.2307/2443468

  38. 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 9:79–100. doi:10.1016/j.ppees.2007.09.001

  39. Kudoh H, Whigham DF (1998) The effect of petal size manipulation on pollinator/seed-predator mediated female reproductive success of Hibiscus moscheutos. Oecologia 117:70–79. doi:10.1007/s004420050633

  40. Lafuma L, Maurice S (2006) Reproductive characters in a gynodioecious species, Silene italica (Caryophyllaceae), with attention to the gynomonoecious phenotype. Biol J Linn Soc Lond 87:583–591. doi:10.1111/j.1095-8312.2006.00597.x

  41. Marshall M, Ganders FR (2001) Sex-biased seed predation and the maintenance of females in a gynodioecious plant. Am J Bot 88:1437–1443. doi:10.2307/3558451

  42. Pettersson MW (1991) Flower herbivory and seed predation in Silene vulgaris (Caryophyllaceae): effects of pollination and phenology. Holarct Ecol 14:45–50

  43. Pettersson MW (1994) Large plant size counteracts early seed predation during the extended flowering season of a Silene uniflora (Caryophyllaceae) population. Ecography 17:264–271. doi:10.1111/j.1600-0587.1994.tb00102.x

  44. Philipp M (1980) Reproductive biology of Stellaria longipes Goldie as revealed by a cultivation experiment. New Phytol 85:557–569. doi:10.1111/j.1469-8137.1980.tb00771.x

  45. Roy BA (1994) The use and abuse of pollinators by fungi. Trends Ecol Evol 9:335–339. doi:10.1016/0169-5347(94)90154-6

  46. SAS Institute (2002) JMP v5.0 user’s guide. SAS Institute, Cary, NC

  47. Shykoff JA, Bucheli E, Kaltz O (1997) Anther smut disease in Dianthus silvester (Caryophyllaceae): natural selection on floral traits. Evolution 51:383–392. doi:10.2307/2411110

  48. Shykoff JA, Kolokotronis S-O, Collin CL, López-Villavicencio M (2003) Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135:1–9

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

  50. Uno GE (1982) Comparative reproductive biology of hermaphroditic and male-sterile Iris douglasiana Herb. (Iridaceae). Am J Bot 69:818–823. doi:10.2307/2442973

  51. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River, New Jersey, USA

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We thank Jessica Franceschina and Marion Cuny, as well as Ñusta Almeida and Annie Collin, remarkable field assistants, for their help in collecting and analyzing data. The Park of the Rupestrian Engravings of Grosio generously allowed us to work on the site, and The Fondazione Fojanini di Studi Superiori (Sondrio, Italy) provided detailed meteorological data. Discussions with the members of the Biodiversity and Ecosystem Functioning team at ENS (Paris) and the Plant Evolutionary Ecology Research Group at the University of Pittsburgh (PA) improved the quality of the manuscript. We wish to thank Laurent Penet, Susan Kephart, Anne Atlan, Isabelle Dajoz, Tia-Lynn Ashman, and the two anonymous reviewers for their insightful comments on the earlier drafts.

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Correspondence to Carine L. Collin.

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Collin, C.L., Shykoff, J.A. Flowering phenology and female fitness: impact of a pre-dispersal seed predator on a sexually polymorphic species. Plant Ecol 206, 1–13 (2010). https://doi.org/10.1007/s11258-009-9620-5

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  • Dianthus sylvestris (Caryophyllaceae)
  • Granivory
  • Gynomonoecy–gynodioecy
  • Hadena
  • Natural enemies
  • Pollination