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So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort

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Abstract

Plant–pollinator interactions are one of the most important and variable mutualisms having major implications for plant fitness. The present study evaluates the interactions between an endemic milkwort, Polygala vayredae, and its floral visitors by studying the temporal variability, foraging behaviour and effectiveness of floral visitors in three populations during three consecutive years. The flowers were visited by a diverse array of insects, totalling 24 different species. However, only four species were effective pollinators, depositing pollen on stigmas after one visit, while the remaining species behaved as nectar robbers, secondary nectar robbers or nectar thieves and were completely ineffective for pollination. Among the effective pollinators, two groups with distinct foraging behaviours were observed: the nectar collecting long-tongued bees Bombus pascuorum and Anthophora sp. and the pollen collectors Eucera longicornis and Halictus sp. No significant differences were observed among pollinators in their efficiency in pollen deposition on stigmas, but significant differences were observed in the foraging behaviour between nectarivorous and pollen collectors. Variation in the abundance and assemblage of floral visitors was observed at the temporal scale and among populations, with the effective pollinators being generally scarce. Consequently, the reproductive outcome in this species was low and significantly variable among populations and years. The results highlight the importance of studying floral visitor effectiveness when determining pollinator assemblages.

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References

  • Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281

    Article  PubMed  Google Scholar 

  • Anderso MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Arizmendi M, Domínguez C, Dirzo R (1996) The role of an avian nectar robber and of hummingbird pollinators in the reproduction of two plant species. Funct Ecol 10:119–127

    Article  Google Scholar 

  • Artz DR, Villagra CA, Raguso RA (2010) Spatiotemporal variation in the reproductive ecology of two parapatric subspecies of Oenothera cespitosa (Onagraceae). Am J Bot 97:1498–1510

    Article  PubMed  Google Scholar 

  • Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421

    Google Scholar 

  • Caruso CM, Peterson SB, Ridley CE (2003) Natural selection on floral traits of Lobelia (Lobeliaceae): spatial and temporal variation. Am J Bot 90:1333–1340

    Article  PubMed  Google Scholar 

  • Castro S, Silveira P, Navarro L (2008a) How flower biology and breeding system affect the reproductive success of the narrow endemic Polygala vayredae Costa (Polygalaceae). Bot J Linn Soc 157:67–81

    Article  Google Scholar 

  • Castro S, Silveira P, Navarro L (2008b) How does secondary pollen presentation affect the fitness of Polygala vayredae (Polygalaceae)? Am J Bot 95:706–712

    Article  PubMed  Google Scholar 

  • Castro S, Silveira P, Navarro L (2008c) Consequences of nectar robbing in the fitness of a threatened plant species. Plant Ecol 199:201–208

    Article  Google Scholar 

  • Castro S, Silveira P, Navarro L, Paiva J, Coutinho AP (2009a) Pollen morphology of Chamaebuxus (DC.) Schb., Chodatia Paiva and Rhinotropis (Blake) Paiva (Polygala L., Polygalaceae). Grana 48:179–192

    Article  Google Scholar 

  • Castro S, Silveira P, Navarro L (2009b) Floral traits variation, legitimate pollination, and nectar robbing in Polygala vayredae (Polygalaceae). Ecol Res 24:47–55

    Article  Google Scholar 

  • Castro S, Silva S, Stanescu I, Silveira P, Navarro L, Santos C (2009c) Pistil anatomy and pollen tube development in Polygala vayredae Costa (Polygalaceae). Plant Biol 11:405–416

    Article  PubMed  CAS  Google Scholar 

  • Dafni A, Kevan P, Husband BC (2005) Practical pollination biology. Enviroquest, Ltr, Cambridge

    Google Scholar 

  • Fenster CB, Dudash MR (2001) Spatiotemporal variation in the role of hummingbirds as pollinators of Silene virginica. Ecology 82:844–851

    Google Scholar 

  • Ferrero V, Castro S, Sánchez JM, Navarro L (2011) Stigma-anther reciprocity, pollinators and pollen transfer efficiency in populations of heterostylous species of Lithodora and Glandora (Boraginaceae). Plant Syst Evol 291:267–276

    Article  Google Scholar 

  • Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304

    Article  Google Scholar 

  • Gómez JM, Zamora R (1999) Generalization vs. specialization in the pollination system of Hormathophylla spinosa (Cruciferae). Ecology 80:796–805

    Google Scholar 

  • Goulson D (2000) Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspect Plant Ecol Evol Syst 2:185–209

    Article  Google Scholar 

  • Guitián J, Guitián P, Navarro L (1996) Spatio-temporal variation in the interactions between Cornus sanguinea and its pollinators. Acta Oecol 17:285–295

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:9

    Google Scholar 

  • Hargreaves AL, Harder LD, Johnson SD (2009) Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biol Rev 84:259–276

    Article  PubMed  Google Scholar 

  • Herrera CM (1988) Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biol J Linn Soc 35:95–125

    Article  Google Scholar 

  • Herrera CM (1989) Pollinator abundance, morphology, and flower visitation rate: analysis of the “quantity” component in a plant-pollinator system. Oecologia 80:241–248

    Google Scholar 

  • Herrera CM (1993) Selection on floral morphology and environmental determinants of fecundity in a hawk moth-pollinated violet. Ecol Monogr 63:251–275

    Article  Google Scholar 

  • Herrera CM, Medrano M, Rey PJ, Sánchez-Lafuente AM, Garcíam MB, Guitián J (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 99:16823–16828

    Article  PubMed  CAS  Google Scholar 

  • Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253

    Article  Google Scholar 

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

    Google Scholar 

  • Irwin RE, Brody A, Waser NM (2001) The impact of floral larceny on individuals, populations, and communities. Oecologia 129:161–168

    Article  Google Scholar 

  • Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev 81:219–235

    Article  PubMed  Google Scholar 

  • Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman TL (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497

    Article  Google Scholar 

  • Moeller DA (2006) Geographic structure of pollinator communities, reproductive assurance, and the evolution of self-pollination. Ecology 87:1510–1522

    Article  PubMed  Google Scholar 

  • Navarro L (1998) Effect of pollen limitation, additional nutrients, flower position and flowering phenology on fruit and seed production in Salvia verbenaca (Lamiaceae). Nord J Bot 18:441–446

    Article  Google Scholar 

  • Navarro L (2000) Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators. Am J Bot 87:980–985

    Article  PubMed  CAS  Google Scholar 

  • Navarro L (2001) Reproductive biology and effect of nectar robbing on fruit production on Macleania bullata (Ericaceae). Plant Ecol 152:59–65

    Article  Google Scholar 

  • Navarro L, Medel R (2009) Relationship between floral tube length and nectar robbing in Duranta erecta L. (Verbenaceae). Biol J Linn Soc 96:392–398

    Article  Google Scholar 

  • Navarro L, Guitián J, Guitián P (1993) Reproductive biology of Petrocoptis grandiflora Rothm. (Caryophyllaceae), a species endemic to the Northwest Iberian Peninsula. Flora 188:253–261

    Google Scholar 

  • Navarro L, Guitián P, Ayensa G (2008) Pollination ecology of Disterigma stereophyllum (Ericaceae) in Southwestern Colombia. Plant Biol 10:512–518

    Article  PubMed  CAS  Google Scholar 

  • Pellmyr O, Thompson JN (1996) Sources of variation in pollinator contribution within a build: the effects of plant and pollinator factors. Oecologia 107:595–604

    Article  Google Scholar 

  • Sahly HF, Conner JK (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brassicaceae). Am J Bot 94:203–209

    Article  Google Scholar 

  • Schemske DW, Horvitz CC (1984) Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225:519–521

    Article  PubMed  CAS  Google Scholar 

  • Schemske DW, Husband BC, Ruckelshaus MH, Goodwillie C, Parker IM, Bishop JG (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:584–606

    Article  Google Scholar 

  • Traveset A, Sáez E (1997) Pollination of Euphorbia dendroides by lizards and insects: spatio-temporal variation in patterns of flower visitation. Oecologia 111:241–248

    Google Scholar 

  • Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environ Entomol 29:413–420

    Article  Google Scholar 

  • Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1070

    Article  Google Scholar 

  • Zhang Y-W, Robert G, Wang Y, Guo Y-H (2007) Nectar robbing of a carpenter bee and its effects on the reproductive fitness of Glechoma longituba (Lamiaceae). Plant Ecol 193:1–13

    Article  Google Scholar 

Download references

Acknowledgments

Authors thank the Departamento de Medi Ambient of Generalitat de Cataluña and the Consorsi d’Alta Garrotxa for allowing this research and to Parc Natural de la Zona Volcànica de la Garrotxa for all the support during field seasons. Authors are grateful to Irina Stanescu for the assistance during 2006 field season and to José M. Gómez for the invaluable help with data analysis and comments during manuscript preparation. Authors are also grateful to the Associate Editor and two anonymous reviewers for the helpful comments to the manuscript. The Portuguese Foundation for Science and Technology financed the work of Sílvia Castro (FCT/BD/10901/2002 and FCT/BPD/41200/2007). Victoria Ferrero was funded by a Xunta de Galicia postdoctoral contract. The work was partially financed under the grants from the Xunta de Galicia (INCITE09-3103009PR), CGL2009-10466 of the Spanish Dirección General de Investigación, Ciencia y Tecnologíca (DGICYT) and FEDER funds from the European Union to Luis Navarro.

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Correspondence to Sílvia Castro.

Appendix 1

Appendix 1

See Table 5.

Table 5 Number of interactions between P. vayredae and its floral visitors in the three populations studied during 2005, 2006 and 2007

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Castro, S., Loureiro, J., Ferrero, V. et al. So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort. Plant Ecol 214, 1233–1245 (2013). https://doi.org/10.1007/s11258-013-0247-1

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