Arthropod-Plant Interactions

, Volume 8, Issue 4, pp 253–260 | Cite as

Pre-dispersal seed predation in gynodioecious Geranium sylvaticum is not affected by plant gender or flowering phenology

  • Sandra Varga
Original Paper


Sex-specific interactions with antagonists may explain female maintenance in gynodioecious populations if seeds produced by hermaphroditic plants are preferred over seeds produced by female plants. Among antagonistic interactions, pre-dispersal seed predators have received relatively little attention even though they may exert sex-specific selective pressures on the evolution of floral and flowering traits. In this work, I investigate temporal variation in seed predation in gynodioecious Geranium sylvaticum, where in addition to female and hermaphrodite individuals, plants with an intermediate sexual expression are also present in most populations. Specifically, I examined whether seed predation is linked to flowering phenology, plant gender, and sexual dimorphism in floral and seed traits over the flowering season using an experimental field population. Within the population, I selected female, intermediate, and hermaphrodite plants with different timing of flowering onset (early, mid, or late), and collected seeds across the fruiting period. Seeds were weighed and examined for seed predator damage. The results show that the three genders experienced similar levels of seed predation attack regardless of their flowering phenology, and that overall seed predation was not related to changes in seed production or seed mass. These results suggest that sexual dimorphism in seed predation cannot be responsible for female maintenance in this species.


Flowering phenology Geranium sylvaticum Gynodioecy Seed predation Zacladus geranii 



I thank Gaia Francini, Emmi Halonen, and Minna-Maarit Kytöviita for help with the practical work, Andrés López-Sepulcre for statistical advice, and Jelmer Elzinga, Rocío Vega-Frutis, and one anonymous referee for commenting on a previous draft of the manuscript. This study was financially supported by the Finnish Academy of Science.


  1. Albrectsen BR (2000) Flowering phenology and seed predation by a tephritid fly: escape of seeds in time and space. Ecoscience 7:433–438Google Scholar
  2. Ashman T-L (2002) The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology 83:1175–1184CrossRefGoogle Scholar
  3. 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 gender dimorphic plant. Am Nat 169:595–608PubMedCrossRefGoogle Scholar
  4. Asikainen E, Mutikainen P (2003) Female frequency and relative fitness of females and hermaphrodites in gynodioecious Geranium sylvaticum (Geraniaceae). Am J Bot 90:226–234PubMedCrossRefGoogle Scholar
  5. Asikainen E, Mutikainen P (2005) Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum. Ann Bot 95:879–886PubMedCrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using s4 classes. R package version 0.999999-0.
  7. Cawthra EM (1957) Notes on the biology of a number of weevils (Col. Curculionidae) occurring in Scotland. Ent Mon Mag 93:204–207Google Scholar
  8. Cipollini ML, Stiles EW (1991) Costs of reproduction in Nyssa sylvatica: sexual dimorphism in reproductive frequency and nutrient flux. Oecologia 86:585–593Google Scholar
  9. Collin CL, Shykoff JA (2003) Outcrossing rates in the gynomonoecious-gynodioecious species Dianthus sylvestris (Caryophyllaceae). Am J Bot 90:579–585PubMedCrossRefGoogle Scholar
  10. Collin CL, Shykoff JA (2010) Flowering phenology and female fitness: impact of a pre-dispersal seed predator on a sexually polymorphic species. Plant Ecol 206:1–13CrossRefGoogle Scholar
  11. 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 131:94–102CrossRefGoogle Scholar
  12. Cornelissen T, Stiling P (2005) Sex-biased herbivory: a meta-analysis of the effects of gender on plant–herbivore interactions. Oikos 111:488–500CrossRefGoogle Scholar
  13. Crawley MJ (1992) Seed predators and plant population dynamics. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford, pp 157–191Google Scholar
  14. Dufaÿ M, Billard E (2012) How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. Ann Bot 109:505–519PubMedCentralPubMedCrossRefGoogle Scholar
  15. Eckhart VM (1992) Resource compensation and the evolution of gynodioecy in Phacelia linearis (Hydrophyllaceae). Evolution 46:1313–1328CrossRefGoogle Scholar
  16. Ehrlén J (1996) Spatiotemporal variation in predispersal seed predation intensity. Oecologia 108:708–713CrossRefGoogle Scholar
  17. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. TREE 22:432–439PubMedGoogle Scholar
  18. Eriksson O (1995) Asynchronous flowering reduces seed predation in the perennial forest herb Actaea spicata. Acta Oecol 16:195–203Google Scholar
  19. Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, UKCrossRefGoogle Scholar
  20. Gómez JM, Zamora R (1994) Top-down effects in a tritrophic system: parasitoids enhance plant fitness. Ecology 75:1023–1030CrossRefGoogle Scholar
  21. Hulme PE, Benkam CW (2002) Granivory. In: Herrera CM, Pellmyr O (eds) Plant-animal interactions: an evolutionary approach. Blackwell, Oxford, pp 132–154Google Scholar
  22. Hultén E, Fries M (1986) Atlas of north European vascular plants north of the tropic of cancer, vol I-III. Koeltz Scientific Books, Königstein, GermanyGoogle Scholar
  23. Jones RW, Peruyero DB (2002) Reproductive ecology of two species of the Anthonomus grandis species group (Coleoptera: Curculionidae) on Hampea (Malvaceae: Gossypieae) host plants in southern Mexico. Environ Entomol 31:693–701CrossRefGoogle Scholar
  24. Kolb A, Ehrlén J, Eriksson O (2007) Ecological and evolutionary consequences of spatial and temporal variation in pre-dispersal seed predation. Perspec Plant Ecol Syst 9:79–100CrossRefGoogle Scholar
  25. Lewis D (1941) Male sterility in natural populations of hermaphroditic plants. New Phytol 40:56–63CrossRefGoogle Scholar
  26. Linkies A, Graeber K, Knight C, Leubner-Metzger G (2010) The evolution of seeds. New Phytol 186:817–831PubMedCrossRefGoogle Scholar
  27. Mahoro S (2002) Individual flowering schedule, fruit set, and flower and seed predation in Vaccinium hirtum Thunb. (Ericaceae). Can J Bot 80:82–92CrossRefGoogle Scholar
  28. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B 273:2575–2584PubMedCentralPubMedCrossRefGoogle Scholar
  29. Marshall M, Ganders FR (2001) Sex-biased seed predation and the maintenance of females in a gynodioecious plant. Am J Bot 88:1437–1443PubMedCrossRefGoogle Scholar
  30. Moles AT, Warton DI, Westoby M (2003) Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 84:3148–3161CrossRefGoogle Scholar
  31. Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Westoby M (2005a) A brief history of seed size. Science 307:576–580PubMedCrossRefGoogle Scholar
  32. Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Pitman AJ, Westoby M (2005b) Factors that shape seed mass evolution. Proc Natl Acad Sci USA 102:10540–10544PubMedCentralPubMedCrossRefGoogle Scholar
  33. Petterson MW (1991) Flower herbivory and seed predation in Silene vulgaris (Caryophyllaceae): effects of pollination and phenology. Holoarctic Ecol 14:45–50Google Scholar
  34. Petterson MW (1992) Advantages of being a specialist female in nodioecious Silene vulgaris S.L. (Caryophyllaceae). Am J Bot 79:1389–1395CrossRefGoogle Scholar
  35. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  36. Rathcke B, Lacey E (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214CrossRefGoogle Scholar
  37. 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 135:1–9PubMedGoogle Scholar
  38. Strauss SE, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Syt 35:435–466CrossRefGoogle Scholar
  39. Tarayre M, Bowman G, Schermann-Legionnet A, Barat M, Atlan A (2007) Flowering phenology of Ulex europaeus: ecological consequences of variation within and among populations. Evol Ecol 21:395–409CrossRefGoogle Scholar
  40. Uno GE (1982) Comparative reproductive biology of hermaphroditic and male-sterile Iris douglasiana Herb. (Iridaceae). Am J Bot 69:818–823CrossRefGoogle Scholar
  41. Vaarama A, Jääskeläinen O (1967) Studies on gynodioecism in the Finnish populations of Geranium sylvaticum L. Ann Acad Scient Fenn A 108:1–39Google Scholar
  42. Varga S, Kytöviita M–M (2014) Variable mycorrhizal benefits on the reproductive output of Geranium sylvaticum, with special emphasis on the intermediate phenotype. Plant Biol 16:306–314PubMedCrossRefGoogle Scholar
  43. Varga S, Vega-Frutis R, Kytöviita M-M (2013) Transgenerational effects of plant sex and arbuscular mycorrhizal symbiosis. New Phytol 199:812–821PubMedCrossRefGoogle Scholar
  44. Volková PA, Rudaková VS, Shipunov AB (2007) Sex ratios in populations of Geranium sylvaticum in European Russia. Plant Spec Biol 22:125–128CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of Biological and Environmental ScienceUniversity of JyväskyläJyväskyläFinland

Personalised recommendations