Skip to main content
Log in

Effects of herbivores and pollinators on fruit yield and survival in a cleistogamous herb

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Although the way in which multiple biotic interactions affect plant reproductive success has been assessed in sexually monomorphic plants, little is known about the joint influence of these interactions on the reproductive success and the consequences to the mating system of plants with sexual heteromorphisms. Dimorphic cleistogamy is a sexual heteromorphism where a single plant produces open, potentially out-crossed chasmogamous (CH) flowers and closed, obligately self-pollinated, cleistogamous (CL) flowers. Fruits produced are also dimorphic with CH fruit being larger and having more seeds than CL fruit. The effects of defoliation and enhancement of the pollination environment on CH and CL fruit yield and plant survival were experimentally assessed in a dimorphic cleistogamous herb (Ruellia nudiflora Engel. & Gray). We predicted that defoliation would have a stronger effect on CH fruit than on CL fruit owing to the high cost of maintaining the former. However, the negative effects of defoliation on CH fruit may be overcome by compensatory mechanisms in an enhanced pollination environment. Lower survival is expected in defoliated plants, particularly in an enhanced pollination environment owing to greater investment in reproduction. As expected, we found that defoliation had a greater negative effect on CH fruit production; however, this effect was absent in the enhanced pollination environment. Enhancement of the pollination environment also increased survival, but only when plants were not defoliated. Although herbivores may increase inbreeding (via reduction of CH fruit production) in plants with dimorphic cleistogamy, this effect may be negligible in environments where pollination service is optimal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdala-Roberts L, Parra-Tabla V, Salinas-Peba L, Herrera C (2009) Noncorrelated effects of seed predation and pollination on the perennial herb Ruellia nudiflora remain spatially consistent. Biol J Linn Soc 96:800–807

    Article  Google Scholar 

  • Abdala-Roberts L, Parra-Tabla V, Salinas-Peba L, Díaz-Castelazo C, Delfín-González H (2010) Spatial variation in the strength of a trophic cascade involving Ruellia nudiflora (Acanthaceae), an insect seed predator and associated parasitoid fauna in Mexico. Biotropica 42:180–187

    Article  Google Scholar 

  • Abdala-Roberts L, Marrufo-Zapata D, Arceo-Gómez G, Parra-Tabla V (2014) Pollen limitation, fruit abortion and autonomous selfing in three populations of Ruellia nudiflora. Plant Species Biol 29:25–33

    Article  Google Scholar 

  • Barber NA, Adler LS, Theis N, Hazzard RV, Kiers T (2012) Herbivory reduces plant interactions with above- and belowground antagonists and mutualists. Ecology 93:1560–1570

    Article  PubMed  Google Scholar 

  • Bell TJ, Quinn JA (1987) Effects of soil moisture and light intensity on the chasmogamous and cleistogamous components of reproductive effort of Dichanthelium clandestinum populations. Can J Bot 65:2243–2249

    Article  Google Scholar 

  • Buchmann SL, Nabhan GP (1996) The forgotten pollinators. Island Press, Washington DC

    Google Scholar 

  • Campbell CS, Quinn JA, Cheplick GP, Bell TJ (1983) Cleistogamy in grasses. Annu Rev Ecol Evol Syst 14:411–441

    Article  Google Scholar 

  • Carr DE, Eubanks MD (2014) Interaction between insect herbivores and plant mating systems. Annu Rev Entomol 59:185–203

    Article  CAS  PubMed  Google Scholar 

  • Cervera JC, Parra-Tabla V (2009) Seed germination and seedling survival traits of invasive and non-invasive congeneric Ruellia species (Acanthaceae) in Yucatan, Mexico. Plant Ecol 205:285–293

    Article  Google Scholar 

  • Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol 34:531–564

    Article  Google Scholar 

  • Crawley MJ (2013) The R book, 2nd edn. John Wiley and Sons Ltd, Chichester

    Google Scholar 

  • Culley TM, Klooster MR (2007) The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms. Bot Rev 73:1–30

    Article  Google Scholar 

  • Dudash MR, Fenster CB (1997) Multiyear study of pollen limitation and cost of reproduction in the iteroparous Silene virginica. Ecology 78:484–493

    Article  Google Scholar 

  • Fujii JA, Kennedy RA (1985) Seasonal changes in the photosynthetic rate in apple trees. A comparison between fruiting and nonfruiting trees. Plant Physiol 78:519–524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • García MB, Ehrlén J (2002) Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population levels. Am J Bot 89:1295–1302

    Article  PubMed  Google Scholar 

  • Gómez JM (2005) Non-additive effects of herbivores and pollinators on Erysimum mediohispanicum (Cruciferae) fitness. Oecologia 143:412–418

    Article  PubMed  Google Scholar 

  • Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol S 36:47–79

    Article  Google Scholar 

  • Hendrix FD (1988) Herbivory and its impact on plant reproduction. In: Lovett-Doust J, Lovett-Doust L (eds) Plant reproductive ecology: patterns and strategies. Oxford University Press, New York, pp 246–265

    Google Scholar 

  • Herrera CM (2000) Measuring the effects of pollinators and herbivores: evidence for non-additivity in a perennial herb. Ecology 81:2170–2176

    Article  Google Scholar 

  • Hladun KR, Adler LS (2009) Influence of leaf herbivory, root herbivory, and pollination on plant performance in Cucurbita moschata. Ecol Entomol 34:144–152

    Article  Google Scholar 

  • Hosmer DW, Lemeshow S, May S (2008) Applied survival analysis: regression model of time to event data, 2nd edn. Wiley and Sons Ltd., New Jersey

    Book  Google Scholar 

  • Le Corff J (1993) Effects of light and nutrient availability on chasmogamy in an understory tropical herb, Calathea micans (Marantaceae). Am J Bot 80:1392–1399

    Article  Google Scholar 

  • Lehtilä K, Syrjänen K (1995) Positive effects of pollination on subsequent size, reproduction, and survival of Primula veris. Ecology 76:1084–1098

    Article  Google Scholar 

  • Long RW (1977) Artificial induction of obligate cleistogamy in species-hybrid in Ruellia (Acanthaceae). Bull Torrey Bot Club 104:53–56

    Article  Google Scholar 

  • Lu Y (2000) Effects of density on mixed mating systems and reproduction in natural populations of Impatiens capensis. Int J Plant Sci 161:671–681

    Article  CAS  Google Scholar 

  • Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B 273:2575–2584

    Article  PubMed Central  PubMed  Google Scholar 

  • Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539

    Article  CAS  PubMed  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 

  • Munguía-Rosas MA, Parra-Tabla V, Ollerton J, Cervera JC (2012) Environmental control of reproductive phenology and the effect of pollen supplementation on resource allocation in the cleistogamous weed, Ruellia nudiflora (Acanthaceae). Ann Bot 109:343–350

    Article  PubMed Central  PubMed  Google Scholar 

  • Munguía-Rosas MA, Abdala-Roberts L, Parra-Tabla V (2013a) Effects of pollen load, parasitoids and the environment on pre-dispersal seed predation in the cleistogamous Ruellia nudiflora. Oecologia 173:871–880

    Article  PubMed  Google Scholar 

  • Munguía-Rosas MA, Parra-Tabla V, Montiel S (2013b) Extreme variation in the reproductive phenology of the weed, Ruellia nudiflora. Weed Res 53:328–336

    Article  Google Scholar 

  • Oakley CG, Maruichi KS, Winn AA (2007) The maintenance of outcrossing in predominantly selfing species: ideas and evidence from cleistogamous species. Annu Rev Ecol Evol S 38:437–457

    Article  Google Scholar 

  • Obeso JR (2002) The cost of reproduction in plants. New Phytol 155:321–348

    Article  Google Scholar 

  • Ortegón-Campos I, Parra-Tabla V, Abdala-Roberts L, Herrera CM (2009) Local adaptation of Ruellia nudiflora (Acanthaceae) to biotic counterparts: complex scenarios revealed when two herbivore guilds are considered. J Evol Biol 22:2288–2297

    Article  PubMed  Google Scholar 

  • Parra-Tabla V, Herrera CM (2010) Spatially inconstant direct and indirect effects of herbivory on floral traits and pollination success in a tropical shrub. Oikos 119:1344–1354

    Article  Google Scholar 

  • Pellmyr O (2002) Pollination by animals. In: Herrera CM, Pellmy O (eds) Plant-animal interactions: an evolutionary approach. Blackwell Publishing, Oxford, pp 157–184

    Google Scholar 

  • Pianka ER (1970) On r- and k selection. Am Nat 104:592–597

    Article  Google Scholar 

  • Quesada M, Bollman K, Stephenson AG (1995) Leaf damage decreases pollen production and hinders pollen performance in Cucurbita texana. Ecology 76:437–443

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing.Vienna: R foundation for statistical computing. http://www.r-project.org/

  • Schemske DW (1978) Evolution of reproductive characteristics in Impatiens (Balsaminaceae): the significance of cleistogamy and chasmogamy. Ecology 59:596–613

    Article  Google Scholar 

  • Schoen DJ, Lloyd DG (1984) The selection of cleistogamy and heteromorphic diaspores. Biol J Linn Soc 23:303–322

    Article  Google Scholar 

  • Schutzenhofer MR (2007) The effect of herbivory on the mating system of congeneric native and exotic Lespedeza species. Int J Plant Sci 168:1021–1026

    Article  Google Scholar 

  • Steets JA, Ashman T-L (2004) Herbivory alters the expression of a mixed-mating system. Am J Bot 91:1046–1051

    Article  PubMed  Google Scholar 

  • Steets JA, Hamrick JL, Ashman T-L (2006) Consequences of vegetative herbivory for maintenance of intermediate outcrossing in an annual plant. Ecology 87:2717–2727

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol S 35:435–466

    Article  Google Scholar 

  • Waller DM (1980) Environmental determinants of outcrossing in Impatiens capensis (Balsaminaceae). Evolution 34:747–761

    Article  Google Scholar 

Download references

Acknowledgments

We thank Jorge Aragón and Armando Rojas for the help in the plant nursery. This research was funded by CINVESTAV (funds to MAM-R). Bianca Delfosse revised the English.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miguel A. Munguía-Rosas.

Additional information

Communicated by Thomas Abeli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Munguía-Rosas, M.A., Arias, L.M., Jurado-Dzib, S.G. et al. Effects of herbivores and pollinators on fruit yield and survival in a cleistogamous herb. Plant Ecol 216, 517–525 (2015). https://doi.org/10.1007/s11258-015-0455-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-015-0455-y

Keywords

Navigation