Skip to main content
SpringerLink
Log in

Comparing the efficiency of pollination mechanisms in Papilionoideae

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

The pump pollination mechanism is typical of basal clades within Papilionoideae and might be associated with less efficient pollen transfer systems, while the explosive tripping mechanism is considered more advanced and might represent the highest expression of the trend in pollen economy. Crotalaria pumila, C. stipularia, Desmodium incanum and D. subsericeum present secondary pollen presentation with pump and explosive pollination mechanisms, respectively. In the present study, we evaluate and compare (1) pollen removal, (2) pollen deposition and (3) pollen transfer efficiency of both mechanisms, considering single visits by Megachile spp., common pollinators of the four plant species in Salta Province, Argentina. Comparisons of visit durations are made in relation to the type of mechanism and rewards offered. We detected significant differences between both mechanisms in the proportion of pollen grains removed and deposited in a flower after a single visit of Megachile. We found that efficiency in pollen transfer was significantly higher for explosive mechanism (2.13 ± 0.42 pollen grains deposited per 100 removed) than for pump mechanism (0.33 ± 0.17 pollen grains deposited per 100 removed). This is the first study that compares efficiency between pollination mechanisms in this group of plants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alemán M (2014) Biología floral, mecanismos de polinización y sistema reproductivo de Papilionoideas nativas del Valle de Lerma (Salta). Tesis de Doctorado en Ciencias Biológicas. Universidad Nacional de Salta

  • Alemán M, Figueroa-Fleming T, Etcheverry A, Sühring S, Ortega-Baes P (2014) The explosive pollination mechanism in Papilionoideae (Leguminosae): an analysis with three Desmodium species. Plant Syst Evol 300:177–186

    Article  Google Scholar 

  • Arroyo MTK (1981) Breeding systems and pollination biology in Leguminosae. In: Polhill RM, Raven PH (eds) Advances in legume systematics, Part 2. Royal Botanic Garden, Kew, pp 723–769

    Google Scholar 

  • Bianchi AR (1996) Temperaturas medias estimadas para la región noroeste de Argentina. INTA, Salta

    Google Scholar 

  • Bianchi AR, Yáñez CE (1992) Las precipitaciones en el noroeste argentino. INTA, Salta

    Google Scholar 

  • Brito VLG, PinheiroM, Sazima M (2010) Sophora tomentosa and Crotalaria vitellina (Fabaceae): reproductive biology and interactions with bees in the restinga of Ubatuba, São Paulo. Biota Neotrop 10: 185–192

    Article  Google Scholar 

  • Castellanos MC, Wilson P, Keller SJ, Wolfe AD, Thomson JD (2006) Anther evolution: pollen presentation strategies when pollinators differ. Am Nat 167:288–296

    Article  PubMed  Google Scholar 

  • Conover WJ (1999) Practical nonparametric statistics. Wiley, New York

    Google Scholar 

  • Córdoba SA, Cocucci AA (2011) Flower power: its association with bee power and floral functional morphology in papilionate legumes. Ann Bot (Lond) 108:919–931

    Article  Google Scholar 

  • Dafni A (1992) The principles of pollination ecology. Oxford University Press, New York

    Google Scholar 

  • Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2010) InfoStat versión 2010. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina

  • Du Puy DJ, Labat JN (2002) Crotalaria. In: Du Puy DJ (ed) The Leguminosae of Madagascar. Royal Botanic Gardens, Kew, pp. 672–708

    Google Scholar 

  • Endress PK (1996) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge

    Google Scholar 

  • Etcheverry AV (2001a) Dynamic dispensing of pollen: an empirical study. In: Proceedings of the 8th international pollination symposium on acta horticulture, vol 561, pp 67–70

  • Etcheverry AV (2001b) Floral biology and pollination in Crotalaria stipularia (Fabaceae: Papilionoideae). In: Proceedings of the 8th international pollination symposium on acta horticulture, vol 561, pp 339–342

  • Etcheverry AV, Protomastro JJ, Westerkamp C (2003) Delayed autonomous self-pollination in the colonizer Crotalaria micans (Fabaceae: Papilionoideae): structural and functional aspects. Plant Syst Evol 239:15–28

    Article  Google Scholar 

  • Etcheverry AV, Alemán MM, Figueroa Fleming T (2008) Flower morphology, pollination biology and mating system of the complex flower of Vigna caracalla (Fabaceae: Papilionoideae). Ann Bot (Lond) 102:305–316

    Article  Google Scholar 

  • Etcheverry AV, Alemán MM, Figueroa-Fleming T, López-Spahr D, Gómez CA, Yáñez C, Figueroa-Castro DM, Ortega-Baes P (2012) Pollen:ovule ratio and its relationship with other floral traits in Papilionoideae (Leguminosae): an evaluation with Argentine species. Plant Biol 14:271–278

    Article  Google Scholar 

  • Faegri K, van der Pijl L (1979) The principles of pollination ecology. 2nd Ed. Pergamon, Oxford

    Google Scholar 

  • Figueroa Fleming T (2014) Interacciones planta-polinizador en Papilionoideas (Leguminosae) simpátricas nativas de Salta, Argentina. Tesis de Doctorado en Ciencias Biológicas. Universidad Nacional de Salta

  • Galen C, Stanton ML (1989) Bumble bee pollination and floral morphology: factors influencing pollen dispersal in the alpine sky pilot, Polemonium viscosum (Polemoniaceae). Am J Bot 76:419–426

    Article  Google Scholar 

  • Galloni M, Cristofolini G (2003) Floral rewards and pollination in Cytiseae (Fabaceae). Plant Syst Evol 238:127–137

    Article  Google Scholar 

  • Galloni M, Podda L, Vivarelli D, Cristofolini G (2007) Pollen presentation, pollen–ovule ratios, and other reproductive traits in Mediterranean legumes (Fam. Fabaceae-Subfam. Faboideae). Plant Syst Evol 266:147–164

    Article  Google Scholar 

  • Harder LD (1990) Pollen removal by bumble bees and its implications for pollen dispersal. Ecology 71:1110–1125

    Article  Google Scholar 

  • Harder LD, Barret SCH (1993) Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology 74:1059–1072

    Article  Google Scholar 

  • Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133:323–344

    Article  Google Scholar 

  • Harder LD, Wilson WG (1994) Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evol Ecol 8:542–559

    Article  Google Scholar 

  • Harder LD, Thomson JD, Cruzan MB, Unnasch RS (1985) Sexual reproduction and variation in floral morphology in an ephemeral vernal lily, Erythronium americanum. Oecologia 67:286–291

    Article  PubMed  Google Scholar 

  • Haynes J, Mesler M (1984) Pollen foraging by bumblebees: Foraging patterns and efficiency on Lupinus polyphyllus. Oecologia 61:249–253

    Article  PubMed  Google Scholar 

  • Herrera CM (1987) Components of pollinator ‘‘quality’’: comparative analysis of a diverse insect assemblage. Oikos 50:79–90

    Article  Google Scholar 

  • Huang L, Jin L, Zhang S, Li J, Yang Y, Zhang X, Wang X (2013) Pollen release mechanisms of papilionaceous plants (Faboideae). Acta Pratacult Sin 22: 305–314

    Google Scholar 

  • Jacobi CM, Ramalho M, Silva M (2005) Pollination biology of the exotic rattleweed Crotalaria retusa L. (Fabaceae) in NE Brazil. Biotropica 37:357–363

    Article  Google Scholar 

  • Juncosa AM, Webster BD (1989) Pollination in Lupinus nanus subsp. latifolius (Leguminosae). Am J Bot 76: 59–66

    Article  Google Scholar 

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot

    Google Scholar 

  • King C, Ballantyne G, Willmer PG (2013) Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol Evol 4:811–818

    Article  Google Scholar 

  • Kittelson PM, Maron JL (2000) Outcrossing rate and inbreeding depression in the perennial yellow bush lupine, Lupinus arboreus (Fabaceae). Am J Bot 87: 652–660

    Article  CAS  PubMed  Google Scholar 

  • Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 54: 575–594

    Article  PubMed  Google Scholar 

  • Le Roux MM, Van Wyk BE (2012) The systematic value of flower structure in Crotalaria and related genera of the tribe Crotalarieae (Fabaceae). Flora 207:414–426

    Article  Google Scholar 

  • Leppik EE (1966) Floral evolution and evolution in Leguminosae. Ann Bot Fennici 3: 99–308

    Google Scholar 

  • López J, Rodríguez-Riaño T, Ortega-Olivencia A, Devesa JA, Ruiz T (1999) Pollination mechanisms and pollen-ovule ratios in some Genisteae (Fabaceae) from Southwestern Europe. Plant Syst Evol 216:23–47

    Article  Google Scholar 

  • Michener CD, Winston ML, Jander R (1978) Pollen manipulation and related activities and structures in bees of the family Apidae. Univ Kansas Sci Bull 51:575–601

    Article  Google Scholar 

  • Ne’eman G, Jurgens A, Newstrom-Lloyd LE, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biol Rev 85:435–451

    PubMed  Google Scholar 

  • Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the worlds: a new map of life on earth. Bioscience 51:933–938

    Article  Google Scholar 

  • Polhill RM (1976) Genisteae (Adans.) Benth. and related tribes (Leguminosae). Syst Bot 1: 143–368

    Google Scholar 

  • Polhill RM (1982) Crotalaria in Africa and Madagascar. A. A. Balkema, Rotterdam

    Google Scholar 

  • Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland

    Google Scholar 

  • Rademaker MCJ, De Jong TJ, Klinkhamer PGL (1997) Pollen dynamics of bumble-bee visitation on Echium vulgare. Funct Ecol 11:554–563

    Article  Google Scholar 

  • Rodríguez-Riaño T, Ortega-Olivencia A, Devesa AJ (1999) Reproductive biology in two Genisteae (Papilionoideae) endemic of the Western Mediterranean Region: Cytisus striatus and Retama sphaerocarpa. Can J Bot 77:809–820

    Google Scholar 

  • Small E (1988) Pollen–ovule patterns in tribe Trifoliae (Leguminosae). Plant Syst Evol 160:195–205

    Article  Google Scholar 

  • Snow AA, Roubik DW (1987) Pollen deposition and removal by bees visiting two tree species in Panama. Biotropica 19:57–63

    Article  Google Scholar 

  • Solomon Raju AJ, Purnachandra Rao S (2006) Explosive pollen release and pollination as a function of nectar-feeding activity of certain bees in the biodiesel plant, Pongamia pinnata (L.) Pierre (Fabaceae). Curr Sci 90: 7–10

    Google Scholar 

  • Stanley DA, Otieno M, Steijven J, Sandler Berlin E, Piiroinen T, Willmer P, Nuttman C (2016) Pollination ecology of Desmodium setigerum (Fabaceae) in Uganda: do big bees do it better? J Pollinat Ecol 19:43–49

    Google Scholar 

  • Suzuki N (2003) Significance of flower exploding pollination on the reproduction of the Scotch broom, Cytisus scoparius (Leguminosae). Ecol Res 18:523–532

    Article  Google Scholar 

  • Thomson JD (1983) Component analysis of community-level interactions in pollination systems. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 451–460

    Google Scholar 

  • Thomson JD, Wilson P, Valenzuela M, Malzone M (2000) Pollen presentation and pollination syndromes, with special reference to Penstemon. Plant Species Biol 15:11–29

    Article  Google Scholar 

  • Thorp RW (1979) Structural, behavioral, and physiological adaptations of bees (Apoidea) for collecting pollen. Ann Mo Bot Gard 66:788–812

    Article  Google Scholar 

  • Westerkamp C (1997) Keel blossoms: bee flowers with adaptations against bees. Flora 192:125–132

    Article  Google Scholar 

  • Westerkamp C, Weber A (1999) Keel flowers of the Polygalaceae and Fabaceae: a functional comparison. Bot J Linn Soc 129:207–221

    Article  Google Scholar 

  • Willmer P, Stanley DA, Steijven K, Matthews IM, Nuttman CV (2009) Bidirectional flower color and shape changes allow a second opportunity for pollination. Curr Biol 19:919–923

    Article  CAS  PubMed  Google Scholar 

  • Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507

    Article  Google Scholar 

  • Yeo PF (1993) Secondary pollen presentation. Form, function and evolution. Springer, New York

    Book  Google Scholar 

  • Young HJ, Stanton ML (1990) Influences of floral variation on pollen removal and seed production in wild radish. Ecology 71:536–547

    Article  Google Scholar 

  • Zych M, Gold J, Stpiczynska M (2013) The most effective pollinator revisited: pollen dynamics in a spring-flowering herb. Arthropod-Plant Interactions 7:315–322

    Article  Google Scholar 

Download references

Acknowledgements

Insects were identified by Dr. Alberto Abrahamovich (Museo de la Plata). Carolina Noemí Yañez and Andrea Florencia Romero helped with field work. The authors thank María Schulze, Francisco Sylvester and Hugo Lesser for their assistance with the English version of the manuscript. This research was supported by grants from Consejo Nacional de Investigaciones Científicas y Técnicas and Consejo de Investigación de la Universidad Nacional de Salta.

Author information

Authors and Affiliations

  1. Facultad de Ciencias Naturales, Universidad Nacional de Salta, Avenida Bolivia 5150, 4400, Salta, Argentina

    Trinidad Figueroa Fleming & Ángela Virginia Etcheverry

Authors
  1. Trinidad Figueroa Fleming
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ángela Virginia Etcheverry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Trinidad Figueroa Fleming.

Additional information

Handling Editor: Isabel Alves dos Santos and Isabel Machado.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Figueroa Fleming, T., Etcheverry, Á.V. Comparing the efficiency of pollination mechanisms in Papilionoideae. Arthropod-Plant Interactions 11, 273–283 (2017). https://doi.org/10.1007/s11829-017-9515-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-017-9515-7

Keywords

Search

Navigation