Sex allocation, pollen limitation and masting in whitebark pine

Journal of Ecology

Volumn 101, Issue 5, 2013, Pages 1345-1352

  Rapp, Joshua M ^a   Mcintire, Eliot J B ^b   Crone, Elizabeth E ^a  

^a HARVARD UNIVERSITY   (United States)

^b PACIFIC FORESTRY CENTRE   (Canada)

Author keywords

Mast seeding; Pinus albicaulis; Pollen coupling; Pollination efficiency; Reproductive ecology; Reproductive synchrony; Seed production; Sex ratio

Indexed keywords

FEMALE; FITNESS; INVESTMENT; MALE; MASTING; MATURATION; MORTALITY; POLLEN LIMITATION; POLLINATION; REPRODUCTIVE EFFORT; REPRODUCTIVE SUCCESS; SEED; SEED DISPERSAL; SEED PRODUCTION; SEX ALLOCATION; SEX RATIO; SURVIVAL; SYNCHRONY; TRADE-OFF; TREE;

MONTANA; UNITED STATES;

PINUS ALBICAULIS;

EID: 84883291325     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12115     Document Type: Article

References (67)

1. Bagchi, R., Philipson, C.D., Slade, E.M., Hector, A., Phillips, S., Villanueva, J.F., Lewis, O.T., Lyal, C.H.C., Nilus, R., Madran, A., Scholes, J.D. & Press, M.C. (2011) Impacts of logging on density-dependent predation of dipterocarp seeds in a South East Asian rainforest. Philosophical Transactions of the Royal Society B-Biological Sciences, 366, 3246-3255.
2. Barringer, L.E., Tomback, D.F., Wunder, M.B. & McKinney, S.T. (2012) Whitebark pine stand condition, tree abundance, and cone production as predictors of visitation by Clark's Nutcracker. PLoS One, 7, 1-11.
3. Bates, D., Maechler, M. & Bolker, B.M. (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42/r1414. http://CRAN.R-project.org/package=lme4
4. Bickel, A.M. & Freeman, D.C. (1993) Effects of pollen vector and plant geometry on floral sex-ratio in monoecious plants. American Midland Naturalist, 130, 239-247.
5. Bierzychudek, P. (1984) Determinants of gender in Jack-in-the-pulpit: the influence of plant size and reproductive history. Oecologia, 65, 14-18.
6. Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. & White, J.-S.S. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution, 24, 127-135.
7. Buonaccorsi, J.P., Elkinton, J., Koenig, W., Duncan, R.P., Kelly, D. & Sork, V. (2003) Measuring mast seeding behavior: relationships among population variation, individual variation and synchrony. Journal of Theoretical Biology, 224, 107-114.
8. Burd, M. & Allen, T.F.H. (1988) Sexual allocation strategy in wind-pollination plants. Evolution, 42, 403-407.
9. Campbell, D.R. (2000) Experimental tests of sex-allocation theory in plants. Trends in Ecology & Evolution, 15, 227-232.
10. Charnov, E.L. (1979) Simultaneous hermaphroditism and sexual selection. Proceedings of the National Academy of Sciences, 76, 2480-2484.
11. Charnov, E.L. (1982) The Theory of Sex Allocation. Princeton University Press, Princeton, New Jersey.
12. Connell, J.H. (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Dynamics of Populations (eds P.J. den Boer & G.R. Gradwell ), pp. 298-310. Centre for Agricultural Publications and Documentation, Wageningen.
13. Crone, E.E., McIntire, E.J.B. & Brodie, J. (2011) What defines mast seeding? Spatio-temporal patterns of cone production by whitebark pine. Journal of Ecology, 99, 438-444.
14. Crone, E.E., Miller, E. & Sala, A. (2009) How do plants know when other plants are flowering? Resource depletion, pollen limitation and mast-seeding in a perennial wildflower. Ecology Letters, 12, 1119-1126.
15. Crone, E.E., Polansky, L. & Lesica, P. (2005) Empirical models of pollen limitation, resource acquisition, and mast seeding by a bee-pollinated wildflower. American Naturalist, 166, 396-408.
16. Davis, H.G., Taylor, C.M., Lambrinos, J.G. & Strong, D.R. (2004) Pollen limitation causes an Allee effect in a wind-pollinated invasive grass (Spartina alterniflora). Proceedings of the National Academy of Sciences of the United States of America, 101, 13804-13807.
17. Dejong, T.J. & Klinkhamer, P.G.L. (1989) Size-dependency of sex-allocation in hermaphroditic, monocarpic plants. Functional Ecology, 3, 201-206.
18. Fernandez-Martinez, M., Belmonte, J. & Maria Espelta, J. (2012) Masting in oaks: disentangling the effect of flowering phenology, airborne pollen load and drought. Acta Oecologica-International Journal of Ecology, 43, 51-59.
19. Friedman, J. & Barrett, S.C.H. (2009) Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Annals of Botany, 103, 1515-1527.
20. Geburek, T., Hiess, K., Litschauer, R. & Milasowszky, N. (2012) Temporal pollen pattern in temperate trees: expedience or fate? Oikos, 121, 1603-1612.
21. Gelman, A. (2008) Scaling regression inputs by dividing by two standard deviations. Statistics in Medicine, 27, 2865-2873.
22. Gelman, A. & Hill, J. (2007) Data Analysis Using Regression and Multilevel/Hierarchical Models. Cambridge University Press, New York.
23. Gelman, A., Su, Y.-S., Yajima, M., Hill, J., Pittau, M.G., Kerman, J. & Zheng, T. (2011) arm: Data analysis using regression and multilevel/hierarchical models. R package version 1.4/14. http://CRAN.R-project.org/package=arm
24. Ghazoul, J. (2005) Pollen and seed dispersal among dispersed plants. Biological Reviews, 80, 413-443.
25. Herrera, C.M., Jordano, P., Guitian, J. & Traveset, A. (1998) Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. American Naturalist, 152, 576-594.
26. Hesse, E. & Pannell, J.R. (2011) Density-dependent pollen limitation and reproductive assurance in a wind-pollinated herb with contrasting sexual systems. Journal of Ecology, 99, 1531-1539.
27. Hutchins, H.E. & Lanner, R.M. (1982) The central role of Clark's nutcracker in the dispersal and establishment of whitebark pine. Oecologia, 55, 192-201.
28. Isagi, Y., Sugimura, K., Sumida, A. & Ito, H. (1997) How does masting happen and synchronize? Journal of Theoretical Biology, 187, 231-239.
29. Janzen, D.H. (1970) Herbivores and the number of tree species in tropical forests. American Naturalist, 104, 501-528.
30. Jewett, J.T., Lawrence, R.L., Marshall, L.A., Gessler, P.E., Powell, S.L. & Savage, S.L. (2011) Spatiotemporal relationships between climate and whitebark pine mortality in the greater Yellowstone ecosystem. Forest Science, 57, 320-335.
31. Jump, A.S. & Penuelas, J. (2006) Genetic effects of chronic habitat fragmentation in a wind-pollinated tree. Proceedings of the National Academy of Sciences of the United States of America, 103, 8096-8100.
32. Kelly, D. (1994) The evolutionary ecology of mast seeding. Trends in Ecology & Evolution, 9, 465-470.
33. Kelly, D., Hart, D.E. & Allen, R.B. (2001) Evaluating the wind pollination benefits of mast seeding. Ecology, 82, 117-126.
34. Kelly, D. & Sork, V.L. (2002) Mast seeding in perennial plants: why, how, where? Annual Review of Ecology and Systematics, 33, 427-447.
35. Klinkhamer, P.G.L., deJong, T.J. & Metz, H. (1997) Sex and size in cosexual plants. Trends in Ecology & Evolution, 12, 260-265.
36. Knapp, E.E., Goedde, M.A. & Rice, K.J. (2001) Pollen-limited reproduction in blue oak: implications for wind pollination in fragmented populations. Oecologia, 128, 48-55.
37. Knops, J.M.H. & Koenig, W.D. (2012) Sex allocation in California Oaks: trade-offs or resource tracking? PLoS One, 7, 1-8.
38. Koenig, W.D., Funk, K.A., Kraft, T.S., Carmen, W.J., Barringer, B.C. & Knops, J.M.H. (2012) Stabilizing selection for within-season flowering phenology confirms pollen limitation in a wind-pollinated tree. Journal of Ecology, 100, 758-763.
39. Korpelainen, H. (1998) Labile sex expression in plants. Biological Reviews, 73, 157-180.
40. Lanner, R.M. (1982) Adaptations of whitebark pine for seed dispersal by Clark's nutcracker. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 12, 391-402.
41. Larson, E.R. (2011) Influences of the biophysical environment on blister rust and mountain pine beetle, and their interactions, in whitebark pine forests. Journal of Biogeography, 38, 453-470.
42. Liebhold, A., Koenig, W.D. & Bjornstad, O.N. (2004) Spatial synchrony in population dynamics. Annual Review of Ecology Evolution and Systematics, 35, 467-490.
43. Lloyd, D.G. & Bawa, K.S. (1984) Modification of the gender of seed plants in varying conditions. Evolutionary Biology, 17, 255-338.
44. Masaka, K. & Takada, T. (2006) Floral sex ratio strategy in wind-pollinated monoecious species subject to wind-pollination efficiency and competitive sharing among male flowers as a game. Journal of Theoretical Biology, 240, 114-125.
45. McDowell, N.G., Beerling, D.J., Breshears, D.D., Fisher, R.A., Raffa, K.F. & Stitt, M. (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology & Evolution, 26, 523-532.
46. McKinney, S.T., Fiedler, C.E. & Tomback, D.F. (2009) Invasive pathogen threatens bird-pine mutualism: implications for sustaining a high-elevation ecosystem. Ecological Applications, 19, 597-607.
47. Meddens, A.J.H., Hicke, J.A. & Ferguson, C.A. (2012) Spatiotemporal patterns of observed bark beetle-caused tree mortality in British Columbia and the western United States. Ecological Applications, 22, 1876-1891.
48. Millar, C.I., Westfall, R.D., Delany, D.L., Bokach, M.J., Flint, A.L. & Flint, L.E. (2012) Forest mortality in high-elevation whitebark pine (Pinus albicaulis) forests of eastern California, USA; influence of environmental context, bark beetles, climatic water deficit, and warming. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 42, 749-765.
49. Montesinos, D., Garcia-Fayos, P. & Verdu, M. (2012) Masting uncoupling: mast seeding does not follow all mast flowering episodes in a dioecious juniper tree. Oikos, 121, 1725-1736.
50. Morgan, P. & Bunting, S.C. (1992) Using cone scars to estimate past cone crops of whitebark pine. Western Journal of Applied Forestry, 7, 71-73.
51. O'Connell, L.M., Mosseler, A. & Rajora, O.P. (2006) Impacts of forest fragmentation on the reproductive success of white spruce (Picea glauca). Canadian Journal of Botany-Revue Canadienne De Botanique, 84, 956-965.
52. Pinheiro, J.C. & Bates, D.M. (2000) Mixed-effect Models in S and S-plus. Springer, New York.
53. Provan, J., Beatty, G.E., Hunter, A.M., McDonald, R.A., McLaughlin, E., Preston, S.J. & Wilson, S. (2008) Restricted gene flow in fragmented populations of a wind-pollinated tree. Conservation Genetics, 9, 1521-1532.
54. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
55. Richardson, D.M. & Rundel, P.W. (1998) Ecology and biogeography of Pinus: an introduction. Ecology and Biogeography of Pinus (ed. D. M. Richardson ), pp. 3-46. Cambridge University Press, Cambridge, UK.
56. Royama, T. (1992) Analytical Population Dynamics. Chapman and Hall Ltd, London, UK.
57. Sakai, S., Harrison, R.D., Momose, K., Kuraji, K., Nagamasu, H., Yasunari, T., Chong, L. & Nakashizuka, T. (2006) Irregular droughts trigger mass flowering in aseasonal tropical forests in Asia. American Journal of Botany, 93, 1134-1139.
58. Sala, A., Hopping, K., McIntire, E.J.B., Delzon, S. & Crone, E.E. (2012) Masting in whitebark pine (Pinus albicaulis) depletes stored nutrients. New Phytologist, 196, 189-199.
59. Satake, A. & Iwasa, Y. (2000) Pollen coupling of forest trees: forming synchronized and periodic reproduction out of chaos. Journal of Theoretical Biology, 203, 63-84.
60. Siepielski, A.M. & Benkman, C.W. (2007) Extreme environmental variation sharpens selection that drives the evolution of a mutualism. Proceedings of the Royal Society B-Biological Sciences, 274, 1799-1805.
61. Silvertown, J.W. (1980) The evolutionary ecology of mast seeding in trees. Biological Journal of the Linnean Society, 14, 235-250.
62. Smith, C.C., Hamrick, J.L. & Kramer, C.L. (1990) The advantage of mast years for wind pollination. American Naturalist, 136, 154-166.
63. Smith, C.M., Wilson, B., Rasheed, S., Walker, R.C., Carolin, T. & Shepherd, B. (2008) Whitebark pine and white pine blister rust in the Rocky Mountains of Canada and northern Montana. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 38, 982-995.
64. Tomback, D.F. (1982) Dispersal of whitebark pine seeds by Clark's nutcracker: a mutualism hypothesis. Journal of Animal Ecology, 51, 451-467.
65. US Fish and Wildlife Service (2011) Endangered and threatened wildlife and plants; 12-month finding on a petition to list Pinus albicaulis as Endangered or Threatened with critical habitat. Federal Register, 76, 42631-42654.
66. Zeglen, S. (2002) Whitebark pine and white pine blister rust in British Columbia, Canada. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 32, 1265-1274.
67. Zhang, D.-Y. (2006) Evolutionarily stable reproductive investment and sex allocation in plants. Ecology and Evolution of Flowers (eds L.D. Harder & C.H. Spencer ), pp. 41-60. Oxford University Press, Oxford.