Nectar yeasts warm the flowers of a winter-blooming plant

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1689, 2010, Pages 1827-1834

  Herrera, Carlos M ^a   Pozo, María I ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

Author keywords

Floral microbiology; Floral microclimate; Helleborus foetidus; Metschnikowia reukaufii; Nectar yeasts; Yeast communities

Indexed keywords

AIR TEMPERATURE; AQUATIC ECOSYSTEM; CATABOLISM; ECOSYSTEM FUNCTION; FLORAL TRAIT; FLOWER VISITING; HERB; NECTAR; NECTARIVORY; POLLINATOR; SUGAR; TERRESTRIAL ECOSYSTEM; WINTER; YEAST;

HELLEBORUS FOETIDUS; HEXAPODA; METSCHNIKOWIA REUKAUFII; RANUNCULACEAE;

EID: 77954337834     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.2252     Document Type: Conference Paper

References (51)

1. Barnett, J. A., Payne, R. W & Yarrow, D. 2000 Yeasts: characteristics and identification, 3rd edn. Cambridge, UK: Cambridge University Press.
2. Boby, V. U., Balakrishna, A. N. & Bagyaraj, D. J. 2008 Interaction between Glomus mosseae and soil yeasts on growth and nutrition of cowpea. Microbiol. Res. 163, 693-700. (doi:10.1016/j.micres.2006.10.004)
3. Brysch-Herzberg, M. 2004 Ecology of yeasts in plantbumblebee mutualism in Central Europe. FEMS Microbiol. Ecol. 50, 87-100. (doi:10.1016/j.femsec.2004. 06.003)
4. Canto, A., Herrera, C. M., Medrano, M., Pérez, R. & García, I. M. 2008 Pollinator foraging modifies nectar sugar composition in Helleborus foetidus L. (Ranunculaceae): an experimental test. Am. J. Bot. 95, 315-320. (doi:10.3732/ajb.95.3.315)
5. Cloete, K. J., Valentine, A. J., Stander, M. A., Blomerus, L. M. & Botha, A. 2009 Evidence of symbiosis between the soil yeast Cryptococcus laurentii and a sclerophyllous medicinal shrub, Agathosma betulina (Berg.) Pillans. Microb. Ecol. 57, 624-632. (doi:10.1007/s00248-008-9457-9)
6. Connell, L., Redman, R., Craig, S., Scorzetti, G., Iszard, M. & Rodriguez, R. 2008 Diversity of soil yeasts isolated from South Victoria Land, Antarctica. Microb. Ecol. 56, 448-459. (doi: 10.1007/s00248-008-9363-1)
7. Cooney, M. J., Marison, I. W., van Gulik, W. M. & von Stockar, U. 1996 Calorimetric and stoichiometric analysis of growth of KLuyveromyces fragilis in continuous culture: nitrogen limitation imposed upon carbon-limited growth. Appl. Microbiol. Biotechnol. 44, 643-653. (doi: 10.1007/BF00172498)
8. Corbett, A. L., Krannitz, P. G. & Aarssen, L. W. 1992 The influence of petals on reproductive success in the Arctic poppy (Papaver radicatum). Can. J. Bot. 70, 200-204. (doi:10.1139/b92-027)
9. de Vega, C., Herrera, C. M. & Johnson, S. D. 2009 Yeasts in floral nectar of some South African plants: quantification and associations with pollinator type. 5. Afr. J. Bot. 75, 798-806. (doi:10.1016/j.sajb.2009.07.016)
10. Dyer, A. G., Whitney, H. M., Arnold, S. E. J., Glover, B. J. & Chittka, L. 2006 Bees associate warmth with floral colour. Nature 442, 525-525. (doi:10.1038/442525a)
11. Gadanho, M. & Sampaio, J. P. 2005 Occurrence and diversity of yeasts in the mid-Atlantic ridge hydrothermal fields near the Azores Archipelago. Microb. Ecol. 50, 408-417. (doi: 10.1007/s00248-005-0195-y)
12. Gadanho, M., Libkind, D. & Sampaio, J. P. 2006 Yeast diversity in the extreme acidic environments of the Iberian Pyrite Belt. Microb. Ecol. 52, 552-563. (doi: 10.1007/ s00248-006-9027-y)
13. Goddard, M. R. 2007 Quantifying the complexities of Saccharomyces cerevisiae's ecosystem engineering via fermentation. Ecology 89, 2077-2082. (doi: 10.1890/072060.1)
14. Gustafsson, L. 1991 Microbiological calorimetry. Thermochim. Acta 193, 145-171. (doi:10.1016/0040-6031(91) 80181-H)
15. Herrera, C. M. 1995 Floral biology, microclimate, and pollination by ectothermic bees in an early-blooming herb. Ecology 76, 218-228. (doi:10.2307/1940644)
16. Herrera, C. M. 2002 Censusing natural microgametophyte populations: variable spatial mosaics and extreme fine-graininess in winter-flowering Helleborus foetidus (Ranunculaceae). Am. J. Bot. 89, 1570-1578. (doi:10. 3732/ajb.89.10.1570)
17. Herrera, C. M., Sánchez-Lafuente, A. M., Medrano, M., Guitián, J., Cerdá, X. & Rey, P. J. 2001 Geographical variation in autonomous self-pollination levels unrelated to pollinator service in Helleborus foetidus (Ranunculaceae). Am. J. Bot. 88, 1025-1032. (doi:10. 2307/2657084)
18. Herrera, C. M., Pérez, R. & Alonso, C. 2006 Extreme intraplant variation in nectar sugar composition in an insect-pollinated perennial herb. Am. J. Bot 93, 575-581. (doi:10.3732/ajb.93.4.575)
19. Herrera, C. M., García, I. M. & Pérez, R. 2008 Invisible floral larcenies: microbial communities degrade floral nectar of bumblebee-pollinated plants. Ecology 89, 2369-2376. (doi:10.1890/08-0241.1)
20. Herrera, C. M., de Vega, C., Canto, A. & Pozo, M. I. 2009 Yeasts in floral nectar: a quantitative survey. Ann. Bot. 103, 1415-1423. (doi:10.1093/aob/mcp026)
21. Herrera, C. M., Canto, A., Pozo, M. I. & Bazaga, P. 2010 Inhospitable sweetness: nectar filtering of pollinatorborne inocula leads to impoverished, phylogenetically clustered yeast communities. Proc. R. Soc. B 277, 747-754. (doi: 10.1098/rspb.2009.1485)
22. Jakobsen, H. B. & Martens, H. 1994 Influence of temperature and ageing of ovules and pollen on reproductive success in Trifolium repens L. Ann. Bot. 74, 493-501. (doi:10.1006/anbo.1994.1146)
23. Kjellberg, B., Karlsson, S. & Kerstensson, I. 1982 Effects of heliotropic movements of flowers of Dryas octopetala L. on gynoecium temperature and seed development. Oecologia 54, 10-13. (doi:10.1007/BF00541101)
24. Krannitz, P. G. 1996 Reproductive ecology of Dryas integrifolia in the high Arctic semi-desert. Can. J. Bot. 74, 1451-1460. (doi:10.1139/b96-175)
25. Kudo, G. 1995 Ecological significance of flower heliotropism in the spring ephemeral Adonis ramosa (Ranunculaceae). Oikos 72, 14-20. (doi: 10.2307/3546032)
26. Lachance, M. A. 2006 Yeast biodiversity: how many and how much? In Biodiversity and ecophysiology of yeasts (eds C. Rosa & G. Péter), pp. 1-9. Berlin, Germany: Springer.
27. Lachance, M. A., Starmer, W. T., Rosa, C. A., Bowles, J. M., Barker, J. S. F. & Janzen, D. H. 2001 Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res. 1, 1-8.
28. Lamprecht, I. 2003 Calorimetry and thermodynamics of living systems. Thermochim. Acta 405, 1-13. (doi: 10. 1016/S0040-6031(03)00123-0)
29. Lamprecht, I., Schmolz, E., Blanco, L. & Romero, C. M. 2002 Flower ovens: thermal investigations on heat producing plants. Thermochim. Acta 391, 107-118. (doi: 10. 1016/S0040-6031 (02)00168-5)
30. Little, A. E. F. & Currie, C. R. 2008 Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89, 1216-1222. (doi:10. 1890/07-0815.1)
31. McKee, J. & Richards, A. J. 1998 Effect of flower structure and flower colour on intrafloral warming and pollen germination and pollen-tube growth in winter flowering Crocus L. (Iridaceae). Bot. J. Linn. Soc. 128, 369-384.
32. Nicolson, S. W., Nepi, M. & Pacini, E. (eds) 2007 Nectaries and nectar. Dordrecht, The Netherlands: Springer.
33. Orueta, D. 2002 Thermal relationships between Calendula arvensis inflorescences and Usia aurata bombyliid flies. Ecology 83, 3073-3085.
34. Patiño, S., Grace, J. & Bänziger, H. 2000 Endothermy by flowers of Rhizanthes lowii (Rafflesiaceae). Oecologia 124, 149-155. (doi:10.1007/s004420050001)
35. Paul, E. A. (ed.) 2007 Soil microbiology and biochemistry, 3rd edn. Oxford, UK: Elsevier.
36. Peay, K. G., Kennedy, P. G. & Bruns, T. D. 2008 Fungal community ecology: a hybrid beast with a molecular master. BioScience 58, 799-810. (doi:10.1641/B580907)
37. Pozo, M. I., de Vega, C., Canto, A. & Herrera, C. M. 2009 Presence of yeasts in floral nectar is consistent with the hypothesis of microbial-mediated signaling in plant-pollinator interactions. Plant Signal. Behav. 4, 1102-1104.
38. Replansky, T., Koufopanou, V., Greig, D. & Bell, G. 2008 Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol. Evol. 23, 494-501. (doi: 10. 1016/j.tree.2008.05.005)
39. Rodrigues, A., Cable, R. N., Mueller, U. G., Bacci, M. & Pagnocca, F. C. 2009 Antagonistic interactions between garden yeasts and microfungal garden pathogens of leafcutting ants. Antonie Van Leeuwenhoek 96, 331-342. (doi:10.1007/s10482-009-9350-7)
40. Sampaio, A., Sampaio, J. P. & Leao, C. 2007 Dynamics of yeast populations recovered from decaying leaves in a nonpolluted stream: a 2-year study on the effects of leaf litter type and decomposition time. FEMS Yeast Res. 7, 595-603. (doi:10.1111/j.1567-1364.2007.00218.x)
41. Sánchez-Lafuente, A. M., Guitián, J., Medrano, M., Herrera, C. M., Rey, P. J. & Cerdá, X. 2005 Plant traits, environmental factors, and pollinator visitation in winter-flowering Helleborus foetidus L. (Ranunculaceae). Ann. Bot. 96, 845-852. (doi:10.1093/aob/mci236)
42. Sapir, Y., Shmida, A. & Ne'eman, G. 2006 Morning floral heat as a reward to the pollinators of the Oncocyclus irises. Oecologia 147, 53-59. (doi: 10.1007/s00442-0050246-6)
43. Seymour, R. S. & Schultze-Motel, P. 1997 Heat-producing flowers. Endeawur 21, 125-129. (doi:10.1016/S01609327(97)80222-0)
44. Seymour, R. S., White, C. R. & Gibernan, M. 2003 Heat reward for insect pollinators. Nature 426, 243-244. (doi:10.1038/426243a)
45. Stanton, M. L. & Galen, C. 1989 Consequences of flower heliotropism for reproduction in an alpine buttercup (Ranunculus adoneus). Oecologia 78, 477-485. (doi:10. 1007/BF00378737)
46. Thompson, J. N. 1988 Variation in interspecific interactions. Ann. Rev. Ecol. Syst. 19, 65-87. (doi:10.1146/annurev.es. 19.110188.000433)
47. Totland, Ø. 1996 Flower heliotropism in an alpine population of Ranunculus acris (Ranunculaceae): effects on flower temperature, insect visitation, and seed production. Am. J. Bot. 83, 452-458. (doi:10.2307/2446214)
48. Vesprini, J. L., Nepi, M. & Pacini, E. 1999 Nectary structure, nectar secretion patterns and nectar composition in two Helleborus species. Plant Biol. 1, 560-568. (doi:10.1111/ j.1438-8677.1999.tb00784.x)
49. Vesprini, J. L., Nepi, M., Ciampolini, F. & Pacini, E. 2008 Holocrine secretion and cytoplasmic content of Helleborus foetidus L. (Ranunculaceae) nectar. Plant Biol. 10, 268271. (doi: 10.1111/j.1438-8677.2007.00023.x)
50. Whitney, H. M., Dyer, A., Chittka, L., Rands, S. A. & Glover, B. J. 2008 The interaction of temperature and sucrose concentration on foraging preferences in bumblebees. Naturwissenschaften 95, 845-850. (doi:10.1007/ s00114-008-0393-9)
51. Wiens, F., Zitzmann, A., Lachance, M. A., Yegles, M., Pragst, F., Wurst, F. M., von Holst, D., Guan, S. L. & Spanagel, R. 2008 Chronic intake of fermented floral nectar by wild treeshrews. Proc. Natl Acad. Sei. USA 105, 10 426-10 431. (doi:10.1073/pnas. 0801628105)