I’ve been robbed! – Can changes in floral traits discourage bee pollination?
Autoři:
Camila Vaz de Souza aff001; Maíra Vidor Salvador aff002; Priscila Tunes aff001; Luiz Claudio Di Stasi aff003; Elza Guimarães aff004
Působiště autorů:
Graduation Program in Biological Sciences, Laboratory of Ecology and Evolution of Plant-Animal Interactions, Department of Botany, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
aff001; Undergraduate Course in Biological Sciences, Laboratory of Ecology and Evolution of Plant-Animal Interactions, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
aff002; Laboratory of Phytomedicine, Pharmacology and Biotechnology, Department of Pharmacology, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
aff003; Laboratory of Ecology and Evolution of Plant-Animal Interactions, Department of Botany, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
aff004
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0225252
Souhrn
Some floral visitors collect nectar by piercing flower external whorls, acting as nectar robbers. They leave robbery vestiges, which can cause changes in floral characteristics, including physical and chemical signals that may influence flower recognition by pollinators. If pollinating bees associate these changes with absence or reduction in nectar volume, they can avoid these flowers, negatively affecting pollination. We aimed to investigate the effect of robbery on primary and secondary attractants. Additionally, we experimentally investigated if the visual signs present in robbed flowers affect the bee pollination of this plant species by discouraging pollinator visits. This study was performed in a very common pollinator-plant-cheaters system comprised by a bee-pollinated Bignoniaceae species and a nectar-robber bee that lands on the corolla tube and makes slits at its base during the nectar robbery. We experimentally isolated the effect of nectar consumption by this nectar-robber and investigated if the slits caused by the nectar-robbers affected the floral scent emission. In addition, we experimentally evaluated the effect of visual signs (slits) associated to the nectar robbery and the effect of nectar depletion on the pollination of Jacaranda caroba (Bignoniaceae). The robbers visited around 75% of the flowers throughout the day and removed significant amounts of nectar from them. However, the damages the robbers cause did not affect floral scent emission and we did not verify significant differences on pollen deposition neither when comparing flowers with slits and control nor when comparing flowers with and without nectar. We showed that even though nectar-robbers visually honestly signal the robbery and deplete high amounts of nectar, they did not affect pollinator visitation. These results showed that presumably antagonistic interactions might in fact not be so.
Klíčová slova:
Bees – Corolla – Flowering plants – Flowers – Pollen – Pollination – Visual signals – Stigma
Zdroje
1. Inouye DW. The terminology of floral larceny. Ecology. 1980;61: 1251–1253.
2. Irwin RE, Bronstein JL, Manson JS, Richardson L. Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol S. 2010;41: 271–292.
3. Hazlehurst JA, Karubian JO. Nectar robbing impacts pollinator behavior but not plant reproduction. Oikos. 2016;125: 1668–1676.
4. Quinalha MM, Nogueira A, Ferreira G, Guimarães E. Effect of mutualistic and antagonistic bees on floral resources and pollination of a savanna shrub. Flora. 2017;232: 30–38.
5. Rojas-Nossa SV, Sánchez JM, Navarro L. Effects of nectar robbing on male and female reproductive success of a pollinator-dependent plant. Ann Bot. 2016;117: 291–297. doi: 10.1093/aob/mcv165 26482653
6. Chittka L, Raine NE. Recognition of flowers by pollinators. Curr Opin Plant Biol. 2006;9(4): 428–435. doi: 10.1016/j.pbi.2006.05.002 16713328
7. Chittka L. Bee cognition. Cur Biol. 2017;27: 1037–1059.
8. Chittka L, Thomson JD. Cognitive Ecology of Pollination–Animal behavior and floral evolution. Cambridge: Cambridge University Press; 2004.
9. Vorobyev M, Gumbert A, Kunze J, Giurfa M, Menzel R. Flowers through insect eyes. Isr J Plant Sci. 1997;45(2–3): 93–101.
10. Wright GA, Schiestl FP. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol. 2009;23: 841–851.
11. Dötterl S, Glück U, Jürgens A, Woodring J, Aas G. Floral reward, advertisement and attractiveness to honey bees in dioecious Salix caprea. PLoS One. 2014;9(3): e93421. doi: 10.1371/journal.pone.0093421 24676333
12. Raguso RA. Why are some floral nectars scented? Ecology. 2004;85(6): 1486–1494.
13. Howell AD, Alarcón R. Osmia bees (Hymenoptera: Megachilidae) can detect nectar-rewarding flowers using olfactory cues. Anim Behav. 2007;74(2): 199–205.
14. Singaravelan N, Nee'man G, Inbar M, Izhaki I. Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. J Chem Ecol. 2005;31(12): 2791–2804. doi: 10.1007/s10886-005-8394-z 16365705
15. Murphy CM, Breed MD. Time-place learning in a Neotropical stingless bee, Trigona fulviventris Guérin (Hymenoptera: Apidae). J Kansas Entomol Soc. 2008;81: 73–77.
16. MacArthur RH, Pianka ER. On optimal use of a patchy environment. Am Nat. 1966;100: 603–609.
17. Genini J, Morellato LPC, Guimarães PR, Olesen J. Cheaters in mutualist networks. Biol Lett. 2010;6: 494–497. doi: 10.1098/rsbl.2009.1021 20089538
18. Melo ACG, Durigan G. Plano de Manejo da Estação Ecológica de Santa Bárbara. São Paulo: Instituto Florestal; 2011.
19. Gottsberger G, Silberbauer-Gottsberger I. Life in the Cerrado–Pollination and Seed Dispersal. Germany: Reta Verlag; 2006.
20. Dafni A, Maués MM. A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod. 1998;11(3): 177–180.
21. Radford AE, Dickson WC, Massey JR, Bell CR. Vascular plant systematics. New York: Haper & Row; 1974.
22. Potts S. Recording pollinator behaviour on flowers. In: Dafni A, Kevan PG, Husband BC, editors. Practical pollination biology. Cambridge: Enviroquest; 2005. p. 330– 339.
23. Dötterl S, Wolfe LM, Jürgens A. Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry. 2005;66: 203–213. doi: 10.1016/j.phytochem.2004.12.002 15652577
24. Adams RP. Identification of essential oil components by gas chromatography/mass spectrometry. 4th ed. Carol Stream, IL: Allured publishing corporation, 2007.
25. Etl F, Berger A, Weber A, Schönenberger J, Dötterl S. Nocturnal plant bugs use cis-Jasmone to locate inflorescences of an Araceae as feeding and mating site. J Chem Ecol. 2016;42: 300–304. doi: 10.1007/s10886-016-0688-9 27074793
26. R Development Core Team, 2018 [cited 25 February 2019]. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, Available from: http://www.R-project.org.
27. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. 2014; arXiv preprint arXiv:1406.5823.
28. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. _nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1–137, <URL: https://CRAN.R-project.org/package=nlme>; 2018.
29. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.5–4. https://CRAN.R-project.org/package=vegan; 2019.
30. Clarke KR, Gorley RN. PRIMER v6: User Manual/Tutorial (Plymouth Routines in Multivariate Ecological Research). PRIMER-E, Plymouth. 2006.
31. Schaefer HM, Ruxton GD. Plant-animal communication. Oxford: Oxford University Press; 2011.
32. Maloof JE, Inouye DW. Are nectar robbers cheaters or mutualists? Ecology. 2000;81: 2651–2661.
33. Laverty TM. Bumble bee learning and flower morphology. Anim Behav.1994;47: 531–545.
34. Chittka L, Thomson JD. Sensori-motor learning and its relevance for task specialization in bumblebees. Behav. Ecol. Sociobiol. 1997;41: 385–398.
35. Rust RW. Pollination of Impatiens capensis: pollinators and nectar robbers. J. Kans. Entomol. Soc. 1979;52: 297–308.
36. Stout JC, Allen JA, Goulson D. Nectar robbing, forager efficiency and seed set: bumblebees foraging on the self incompatible plant Linaria vulgaris (Scrophulariaceae). Acta Oecol.-Int. J. Ecol. 2000;21:277–83.
37. Richardson SC. Are nectar-robbers mutualists or antagonists? Oecologia. 2004;139: 246–54. doi: 10.1007/s00442-004-1504-8 14767755
38. Singh VK, Barman C, Tandon R. Nectar robbing positively influences the reproductive success of Tecomella undulata (Bignoniaceae). PloS One. 2014;9(7): e102607. doi: 10.1371/journal.pone.0102607 25036554
39. Maloof JE. The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am J Bot. 2001;88(11): 1960–1965. 21669629
40. DeBenedictis PA, Gill FB, Hainsworth FR, Pyke GH, Wolf LL. Optimal meal size in hummingbirds. The Am Nat. 1978;112(984): 301–316.
41. Hodges CM, Wolf LL. Optimal foraging in bumblebees: why is nectar left behind in flowers?. Behav Ecol Sociobiol, 1981;9(1), 41–44.
42. Schiestl FP, Johnson SD. Pollinator-mediated evolution of floral signals. Trends Ecol Evol. 2013;28(5): 307–315. doi: 10.1016/j.tree.2013.01.019 23480953
43. Parachnowitsch AL, Manson JS, Sletvold N. Evolutionary ecology of nectar. Ann Bot. 2018;123: 247–261.
44. Bronstein JL, Alarcón R, Geber M. The evolution of plant–insect mutualisms. New Phytol. 2006;172(3), 412–428. doi: 10.1111/j.1469-8137.2006.01864.x 17083673
45. Raguso RA. Floral scent, olfaction, and scent-driven foraging behavior. In: Chittka L, Thomson JD, editors. Cognitive Ecology of Pollination–Animal behavior and floral evolution. Cambridge: Cambridge University Press; 2001.
46. Dobson HEM, Raguso RA, Knudsen JT, Ayasse M. Scent as an attractant. In: Dafni A, Kevan PG, Husband BC, editors. Practical Pollination Biology. Cambridge: Enrivoquest; 2005. p. 197–230.
47. Kunze J, Gumbert A. The combined effect of color and odor on flower choice behavior of bumble bees in flower mimicry systems. Behav Ecol. 2001;12: 447–456.
48. Guimarães E, Tunes P, de Almeida Junior LD, Di Stasi LC, Dötterl S, Machado SR. Nectar replaced by volatile secretion: a potential new role for nectarless flowers in a bee-pollinated plant species. Front Plant Sci. 2018;9: 1243. doi: 10.3389/fpls.2018.01243 30233609
49. Zimmerman M, Cook S. Pollinator foraging, experimental nectar robbing and plant fitness in Impatiens capensis. Am Midl Nat. 1985;113: 84–91.
50. Irwin RE, Howell P, Galen C. Quantifying direct vs. indirect effects of nectar robbers on male and female components of plant fitness. J Ecol. 2015;103: 1487–497.
51. Wu Y, Zhang ZQ, Li QJ. Nectar robbers influence the trait–fitness relationship of Primula secundiflora. Plant Biol. 2019;21: 967–974. doi: 10.1111/plb.13000 31050864
52. Murphy CM, Breed MD. Nectar and resin robbing in stingless bees. Am. Entomol. 2008;54(1): 36–44.
Článek vyšel v časopise
PLOS One
2019 Číslo 11
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Je libo čepici místo mozkového implantátu?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
Nejčtenější v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy