Pollination mode predicts phenological response to climate change in terrestrial orchids: A case study from central Europe

Journal of Ecology

Volumn 100, Issue 5, 2012, Pages 1141-1152

  Molnár V, Attila ^a   Tökölyi, Jácint ^a   Végvári, Zsolt ^b   Sramkó, Gábor ^c,d   Sulyok, József ^e   Barta, Zoltán ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIV OF HORT AND FOOD INDUSTRY   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d UNIVERSITY OF READING   (United Kingdom)

^e Bukki Nemzeti Park   (Hungary)

Author keywords

Biological collections; Flowering time; Global change; Herbarium specimens; Life history; Life span; Orchidaceae; Phenological shift; Phylogenetic control; Plant climate interactions; Pollinator

Indexed keywords

BIOGEOGRAPHY; CLIMATE CHANGE; DATA SET; GLOBAL CHANGE; HERB; LIFE HISTORY TRAIT; NUMERICAL MODEL; PHENOLOGY; PHYLOGENETICS; PHYSIOLOGICAL RESPONSE; PLANT-POLLINATOR INTERACTION; POLLINATION; POPULATION DISTRIBUTION; RELATEDNESS; TAXONOMY; TERRESTRIAL ENVIRONMENT;

HUNGARY;

EID: 84865294272     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/j.1365-2745.2012.02003.x     Document Type: Article

References (78)

1. Ahas, R., Aasa, A., Menzel, A., Fedotova, V.G. & Scheifinger, H. (2002) Changes in European spring phenology. International Journal of Climatology, 22, 1727-1738.
2. Anderson, S.H., Kelly, D., Ladley, J.J., Molloy, S. & Terry, J. (2011) Cascading effects of bird functional extinction reduce pollination and plant density. Science, 331, 1068-1071.
3. Araújo, M.B. & Luoto, M. (2007) The importance of biotic interactions for modelling species distributions under climate change. Global Ecology and Biogeography, 16, 743-753.
4. Askeyev, O.V., Sparks, T.H., Askeyev, I.V., Tishin, D.V. & Tryjanowski, P. (2010) East versus West: contrasts in phenological patterns? Global Ecology and Biogeography, 19, 783-793.
5. Baker, H.G. (1974) The evolution of weeds. Annual Review of Ecology and Systematics, 5, 1-24.
6. Baldwin, B.G., Sanderson, M.J., Porter, J.M., Wojciechowski, M.F., Campbell, C.S. & Donoghue, M.J. (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden, 82, 247-277.
7. Bartomeus, I., Ascher, J.A., Wagner, D., Danfortd, B.N., Colla, S., Kornbluth, S. & Winfree, R. (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proceedings of the National Academy of Sciences of the United States of America, 108, 20645-20649.
8. Bateman, R.M., Smith, R.J. & Fay, M.F. (2008) Morphometric and population genetic analyses elucidate the origin, evolutionary significance and conservation implications of Orchis × angusticruris (O. purpurea × O. simia), a hybrid orchid new to Britain. Botanical Journal of the Linnean Society, 157, 687-711.
9. Bateman, R.M., Hollingsworth, P.M., Preston, J., Lou, Y.B., Pridgeon, A.M. & Chase, M.W. (2003) Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society, 142, 1-40.
10. Bateman, R.M., Hollingsworth, P.M., Squirrell, J. & Hollingsworth, M.L. (2005) Tribe Neottieae. Phylogenetics. Genera Orchidacearum, Volume 4. Epidendroideae (part one) (eds A.M. Pridgeon, P.J. Cribb, M.W. Chase & F.N. Rasmussen ), pp. 487-495. Oxford University Press, Oxford.
11. Bonan, G.B. (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science, 320, 1444-1449.
12. Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer Verlag, New York, NY.
13. Claessens, J. & Kleynen, J. (2011) The Flower of the European Orchid. Form and Function. Jean Claessens & Jacques Kleynen, Geuelle.
14. Cleland, E.E., Chuine, I., Menzel, A., Mooney, H.A. & Schwartz, M.D. (2007) Shifting plant phenology in response to global change. Trend in Ecology & Evolution, 22, 357-365.
15. Dafni, A. (1984) Mimicry and deception in pollination. Annual Review of Ecology, Evolution, and Systematics, 15, 259-278.
16. Davis, C.C., Willis, C.G., Primack, R.B. & Miller-Rushing, A.J. (2010) The importance of phylogeny to the study of phenological response to global climate change. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365, 3201-3213.
17. Dixon, K.W. (2009) Pollination and restoration. Science, 325, 571-573.
18. Dunne, J.A., Harte, J. & Taylor, K.J. (2003) Subalpine meadow flowering phenology responses to climate change: Integrating experimental and gradient methods. Ecological Monographs, 73, 69-86.
19. Fitter, A.H. & Fitter, R.S.R. (2002) Rapid changes in flowering time in British plants. Science, 296, 1689-1691.
20. Forrest, J. & Miller-Rushing, A.J. (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365, 3101-3112.
21. Freckleton, R.P., Harvey, P.H. & Pagel, M. (2002) Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist, 160, 712-726.
22. Gienapp, P., Leimu, R. & Merilä, J. (2007) Responses to climate change in avian migration time - microevolution versus phenotypic plasticity. Climate Research, 35, 25-35.
23. Gulyás, G., Sramkó, G., Molnár V ., A., Rudnóy, S., Illyés, Z., Balázs, T. & Bratek, Z. (2005) Nuclear ribosomal DNA ITS paralogs as evidence of recent interspecific hybridization in the genus Ophrys (Orchidaceae). Acta Biologica Cracoviensia Series Botanica, 47, 61-67.
24. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
25. Harmon, L., Weir, J., Brock, C., Glor, R., Challenger, W. & Hunt, G. (2009). geiger: Analysis of evolutionary diversification. R package version 1.3-1. http://CRAN.R-project.org/package=geiger
26. Hegland, S.J., Nielsen, A., Lázaro, A., Bjerknes, A.L. & Totland, Ø. (2009) How does climate warming affect plant-pollinator interactions? Ecology Letters, 12, 184-195.
27. Hoffmann, A.A. & Sgrò, C.M. (2011) Climate change and evolutionary adaptation. Nature, 470, 479-485.
28. Horváth, F., Dobolyi, Z.K., Morschhauser, T., Lo{double acute}kös, L., Karas, L. & Szerdahelyi, T. (1995) Flóra Database 1.2. Ecological and Botanical Institute of the Hungarian Academy of Sciences, Vácrátót, Hungary.
29. Internicola, A.I., Bernasconi, G. & Gigord, L.D. (2008) Should food-deceptive species flower before or after rewarding species? An experimental test of pollinator visitation behaviour under contrasting phenologies. Journal of Evolutionary Biology, 21, 1358-1365.
30. Internicola, A.I. & Harder, L.D. (2012) Bumble-bee learning selects for both early and long flowering in food-deceptive plants. Proceedings of the Royal Society of London. Series B, 279, 1538-1543.
31. IPCC. (2007) Intergovernmental Panel on Climate Change: Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
32. Jacquemyn, H., Brys, R., Honnay, O. & Hutchings, M.J. (2002) Orchis mascula (L.) L. Biological Flora of the British Isles No. 252. Journal of Ecology, 97, 360-377.
33. Jacquemyn, H., Brys, R., Hermy, M. & Willems, J.H. (2005) Does nectar reward affect rarity and extinction probabilities of orchid species? An assessment using historical records from Belgium and the Netherlands. Biological Conservation, 121, 257-263.
34. Jersáková, J., Johnson, S.D. & Kindlmann, P. (2006) Mechanisms and evolution of deceptive pollination in orchids. Biological Reviews, 81, 219-235.
35. Jump, A.S. & Peñuelas, J. (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters, 8, 1010-1020.
36. Kull, T. & Hutchings, M.J. (2006) A comparative analysis of decline in the distribution ranges of orchid species in Estonia and the United Kingdom. Biological Conservation, 129, 31-39.
37. Lenoir, J., Gegout, J.C., Marquet, P.A., de Ruffray, P. & Brisse, H. (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science, 320, 1768-1771.
38. Martins, E.P. & Hansen, T.F. (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist, 149, 646-667.
39. Menzel, A., Sparks, T.H., Estrella, N. & Roy, D.B. (2006) Altered geographic and temporal variability in phenology in response to climate change. Global Ecology and Biogeography, 15, 498-504.
40. Miller-Rushing, A.J., Inouye, D.W. & Primack, R.B. (2008) How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. Journal of Ecology, 96, 1289-1296.
41. Miller-Rushing, A.J. & Primack, R.B. (2008) Global warming and flowering times in Thoreau's Concord: a community perspective. Ecology, 89, 332-341.
42. Miller-Rushing, A.J., Primack, R.B., Primack, D. & Mukunda, S. (2006) Photographs and herbarium specimens as tools to document phenological changes in response to global warming. American Journal of Botany, 93, 1667-1674.
43. Molnár V ., A. (ed.) (2011) Magyarország orchideáinak atlasza [Atlas of Hungarian Orchids]. Kossuth Kiadó, Budapest.
44. Molnár V ., A., Takács, A., Horváth, O., Vojtkó, A.E., Király, G., Sonkoly, J. & Sramkó, G. (2012) Herbarium Database of Hungarian Orchids I. Methodology, dataset, historical aspects and taxa. Biologia, 67, 79-86.
45. Neiland, M.R.M. & Wilcock, C.C. (1999) Fruit set, nectar reward, and rarity in the Orchidaceae. American Journal of Botany, 85, 1657-1671.
46. Orme, D., Freckleton, R., Thomas, G., Petzoldt, T. & Fritz, F. (2009) CAIC: Comparative Analyses using Independent Contrasts. http://R-Forge.R-project.org/projects/caic/
47. Pagel, M. (1997) Inferring evolutionary processes from phylogenies. Zoologica Scripta, 26, 331-348.
48. Pagel, M. (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology, 48, 612-622.
49. Panchen, Z.A., Primack, R.B., Anisko, T. & Lyons, R.E. (2012) Herbarium specimens, photographs, and field observations show Philadelphia area plants are responding to climate change. American Journal of Botany, 99, 751-756.
50. Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics, 37, 637-669.
51. Parmesan, C. & Yohe, G. (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
52. Paun, O., Bateman, R.M., Fay, M.F., Hedrén, M., Civeyler, L. & Chase, M.W. (2010) Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Molecular Biology and Evolution, 27, 2465-2473.
53. Paun, O., Bateman, R.M., Fay, M.F., Luna, J.A., Moat, J., Hedrén, M. & Chase, M.W. (2011) Altered gene expression and ecological divergence in sibling allopolyploids of Dactylorhiza (Orchidaceae). BMC Evolutionary Biology, 11, 113.
54. Pellissier, L., Vittoz, P., Internicola, A.I. & Gigord, L.D.B. (2010) Generalized food-deceptive orchid species flower earlier and occur at lower altitudes than rewarding ones. Journal of Plant Ecology, 3, 243-250.
55. Post, E.S., Pedersen, C., Wilmers, C.C. & Forchhammer, M.C. (2008) Phenological sequences reveal aggregate life-history response to climatic warming. Ecology, 89, 363-370.
56. Prather, L.A., Alvarez-Fuentes, O., Mayfield, M.H. & Fergusson, C.J. (2004) The decline of plant collecting in the United States: a threat to the infrastructure of biodiversity studies. Systematic Botany, 29, 15-28.
57. Price, M.W. & Waser, N.M. (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology, 79, 1261-1271.
58. Primack, R.B. & Miller-Rushing, A.J. (2009) The role of botanical gardens in climate change research. New Phytologist, 182, 303-313.
59. Primack, R.B. & Miller-Rushing, A.J. (2011) Broadening the study of phenology and climate change. New Phytologist, 191, 307-309.
60. R Development Core Team. (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
61. Rafferty, N.E. & Ives, A.R. (2011) Effects of experimental shifts in flowering phenology on plant-pollinator interactions. Ecology Letters, 14, 69-74.
62. Robbirt, K.M., Davy, A.J., Hutchings, M.J. & Roberts, D.L. (2011) Validation of biological collections as a source of phenological data for use in climate change studies: a case study with the orchid Ophrys sphegodes. Journal of Ecology, 99, 235-241.
63. Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C. & Pounds, J.A. (2003) Fingerprints of global warming on wild animals and plants. Nature, 421, 57-60.
64. Sanderson, M.J. (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics, 19, 301-302.
65. Schiestl, F.P. (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften, 92, 255-264.
66. Schröter, D., Cramer, W., Leemans, R., Prentice, I.C., Araújo, M.B., Arnell, N.W. et al. (2005) Ecosystem service supply and vulnerability to global change in Europe. Science, 310, 1333-1337.
67. Schwartz, M.D., Ahas, R. & Aasa, A. (2006) Onset of spring starting earlier across the Northern hemisphere. Global Change Biology, 12, 343-351.
68. Sherry, R.A., Zhou, X.H., Gu, S.L., Arnone, J.A., Schimel, D.S., Verburg, P.S., Wallace, L.L. & Luo, Y. (2007) Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences of the United States of America, 104, 198-202.
69. Sparks, T.H., Jeffree, E.P. & Jeffree, C.E. (2000) An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. International Journal of Biometeorology, 44, 82-87.
70. Sparks, T.H. & Menzel, A. (2002) Observed changes in seasons: an overview. International Journal of Climatology, 22, 1715-1725.
71. Swarts, N.D. & Dixon, K.W. (2009) Terrestrial orchid conservation in the age of extinction. Annals of Botany, 104, 543-556.
72. Swofford, D.L. (2002) PAUP. Phylogenetic Analysis Using Parsimony (and Other Methods). Version 4. Sinauer Associates, Sunderland, MA.
73. Vallius, E. (2000) Position-dependent reproductive success of flowers in Dactylorhiza maculata. (Orchidaceae). Functional Ecology, 14, 573-579.
74. Végvári, Z., Bókony, V., Barta, Z. & Kovács, G. (2010) Life-history predicts advancement of avian spring migration in response to climate change. Global Change Biology, 16, 1-11.
75. Walther, G.R. (2004) Plants in a warmer world. Perspectives in Plant Ecology, Evolution, and Systematics, 6, 169-185.
76. Walther, G.R. (2010) Community and ecosystem responses to recent climate change. Philosophical Transactions of the Royal Society of London Series B, 365, 2019-2024.
77. Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.-M., Hoegh-Guldberg, O. & Bairlein, F. (2002) Ecological responses to recent climate change. Nature, 416, 389-395.
78. Willis, C.G., Ruhfel, B., Primack, R.B., Miller-Rushing, A.J. & Davis, C.C. (2008) Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proceedings of the National Academy of Sciences of the United States of America, 105, 17029-17033.