DOI QR코드

DOI QR Code

The optimal balance between sexual and asexual reproduction in variable environments: a systematic review

  • Yang, Yun Young (Graduate School of Interdisciplinary Program in Environmental Education, Seoul National University) ;
  • Kim, Jae Geun (Graduate School of Interdisciplinary Program in Environmental Education, Seoul National University)
  • Received : 2016.09.01
  • Accepted : 2016.11.07
  • Published : 2016.11.30

Abstract

Many plant species have two modes of reproduction: sexual and asexual. Both modes of reproduction have often been viewed as adaptations to temporally or spatially variable environments. The plant should adjust partitioning to match changes in the estimated success of the two reproductive modes. Perennial plants showed that favorable habitats in soil nutrients or water content tend to promote clonal growth over sexual reproduction. In contrast, under high light-quantity conditions, clonal plants tend to allocate more biomass to sexual reproduction and less to clonal propagation. On the other hand, plants with chasmogamous and cleistogamous flowers provides with a greater tendency of the opportunity to ensure some seed set in any stressful environmental conditions such as low light, low soil nutrients, or low soil moisture. It is considered that vegetative reproduction has high competitive ability and is the major means to expand established population of perennial plants, whereas cleistogamous reproduction is insurance to persist in stressful sites due to being strong. Chasmogamous reproduction mainly enhances established and new population. Therefore, the functions of sexual and asexual propagules of perennial or annual plants differ from each other. These traits of propagule thus determine its success at a particular region of any environmental gradients. Eventually, if environmental resources or stress levels change in either space or time, species composition will probably also change. The reason based on which the plants differ with respect to favored reproduction modes in each environmental condition, may be involved in their specific realized niche.

Keywords

References

  1. Alvarez, M. G., Tron, F., & Mauchamp, A. (2005). Sexual versus asexual colonization by Phragmites australis: 25-year reed dynamics in a Mediterranean marsh, southern France. Wetlands, 25, 639-647. https://doi.org/10.1672/0277-5212(2005)025[0639:SVACBP]2.0.CO;2
  2. Antlfinger, A. E. (1986). Field germination and seedling growth of CH and CL progeny of Impatiens apensis (Balsaminaceae). American Journal of Botany, 73, 1267-1273. https://doi.org/10.2307/2444061
  3. Bai, W., Sun, X., Wang, Z., & Li, L. (2009). Nitrogen addition and rhizome severing modify clonal growth and reproductive modes of Leymus chinensis population. Plant Ecology, 205, 13-21. https://doi.org/10.1007/s11258-009-9595-2
  4. Baker, H. G. (1974). The evolution of weeds. Annual review of ecology and systematics, 5, 1-24. https://doi.org/10.1146/annurev.es.05.110174.000245
  5. Bazzaz, F. A. (1997). Allocation of resources in plants: state of the science and critical questions. In F. A. Bazzaz & J. Grace (Eds.), Plant resource allocation (pp. 1-37). London: Academic.
  6. Bazzaz, F. A., & Ackerly, D. D. (1992). Reproductive allocation and reproductive effort in plants. In M. Fenner (Ed.), Seeds: the ecology of regeneration in plant communities (pp. 1-26). Oxon: CAB International.
  7. Bazzaz, F. A., Chiariello, N. R., Coley, P. D., & Pitelka, L. F. (1987). Allocating resources to reproduction and defense. Bioscience, 37(1), 58-67. https://doi.org/10.2307/1310178
  8. Beattie, A. J. (1971). Itinerant pollinators in a forest. Madrofio, 21, 120-124.
  9. Bell, T. J., & Quinn, J. A. (1987). Effects of soil moisture and light intensity on the chasmogamous and cleistogamous components of reproductive effort of Dichanthelium clandestinum populations. Canadian Journal of Botany, 65, 2243-2249. https://doi.org/10.1139/b87-305
  10. Berendse, F. (1998). Effects of dominant plant species on soils during succession in nutrient-poor ecosystems. Biogeochemistry, 42, 73-88. https://doi.org/10.1023/A:1005935823525
  11. Boedeltje, G., Ozinga, W. A., & Prinzing, A. (2008). The trade-off between vegetative and generative reproduction among angiosperms influences regional hydrochorous propagule pressure. Global Ecology and Biogeography, 17, 50-58.
  12. Brown, W. V. (1952). The relation of soil moisture to cleistogamy in Stipa leucotricha. Botanical Gazette, 113(4), 438-444. https://doi.org/10.1086/335732
  13. Callaghan, T. V. (1984). Growth and translocation in a clonal southern hemisphere sedge, Uncinia meridensis. Journal of Ecology, 72, 529-546. https://doi.org/10.2307/2260064
  14. Campbell, C. S., Quinn, J. A., Cheplick, G. P., & Bell, T. J. (1983). Cleistogamy in grasses. Annual Review of Ecological Systems, 14, 411-441. https://doi.org/10.1146/annurev.es.14.110183.002211
  15. Ceplitis, A. (2001). The importance of sexual and asexual reproduction in the recent evolution of Allium vineale. Evolution, 55, 1581-1591. https://doi.org/10.1111/j.0014-3820.2001.tb00677.x
  16. Chen, X., Li, Y., Xie, Y., Deng, Z., Li, X., Li, F., & Hou, Z. (2015). Trade-off between allocation to reproductive ramets and rhizome buds in Carex brevicuspis populations along a small-scale elevational gradient. Science Reports, 5, 12688. doi:10.1038/srep12688.
  17. Cheplick, G. P. (1989). Nutrient availability, dimorphic seed production, and reproductive allocation in the annual grass Amphicarpum purshii. Canadian Journal of Botany, 67, 2514-2521. https://doi.org/10.1139/b89-321
  18. Cheplick, G. P. (1994). Life history evolution in amphicarpic plants. Plant Species Biology, 9, 119-131. https://doi.org/10.1111/j.1442-1984.1994.tb00092.x
  19. Cheplick, G. P. (1995). Life history trade-offs in Aphibromus scabrivalvis (Poaceac): allocation to clonal growth, storage, and cleistogamous reproduction. American Journal of Botany, 82, 621-629. https://doi.org/10.2307/2445420
  20. Cheplick, G. P. (1996). Cleistogamy and seed heteromorphism in Triplasis purpurea (Poaceae). Bulletin of the Torrey Botanical Club, 123, 25-33. https://doi.org/10.2307/2996303
  21. Cheplick, G. P. (2005). Biomass partitioning and reproductive allocation in the invasive, cleistogamous grass Microstegium vimineum: influence of the light environment. The Journal of the Torrey Botanical Society, 132, 214-224. https://doi.org/10.3159/1095-5674(2005)132[214:BPARAI]2.0.CO;2
  22. Cheplick, G. P. (2007). Plasticity of chasmogamous and cleistogamous reproductive allocation in grasses. A Journal of Systematic and Evolutionary Botany, 23, 286-294.
  23. Cheplick, G. P., & Quinn, J. A. (1982). Amphicarpum purshii and the “pessimistic strategy” in amphicarpic annuals with subterranean fruit. Oecologia, 52, 327-332. https://doi.org/10.1007/BF00367955
  24. Choo, Y. H., Nam, J. M., Kim, J. H., & Kim, J. G. (2015). Advantages of amphycarpy of Persicaria thunbergii in the early life history. Aquatic Botany, 121, 33-38. https://doi.org/10.1016/j.aquabot.2014.11.001
  25. Chu, Y., Yu, F. H., & Dong, M. (2006). Clonal plasticity in response to reciprocal patchiness of light and nutrients in the stoloniferous herb Glechoma longituba L. Journal of Integrative Plant Biology, 48, 400-408. https://doi.org/10.1111/j.1744-7909.2006.00237.x
  26. Chung, M. G., & Epperson, B. K. (1999). Spatial holdfastic structure of clonal and sexual reproduction in populations of Adenophora grandiflora (Campanulaceae). Evolution, 53, 1068-1078. https://doi.org/10.1111/j.1558-5646.1999.tb04522.x
  27. Clark, D. A., & Clark, D. B. (1987). Temporal and environmental patterns of reproduction in Zamia skinneri, a tropical rain forest cycad. Journal of Ecology, 75, 135-149. https://doi.org/10.2307/2260540
  28. Corff, J. L. (1993). Effects of light and nutrient availability on chasmogamy and cleistogamy in an understory tropical herb, Calathea micans (Marantaceae). American Journal of Botany, 80, 1392-1399. https://doi.org/10.2307/2445667
  29. Culley, T. M. (2002). Reproductive biology and delayed selfing in Viola pubescens (Violaceae), an understory herb with chasmogamous and cleistogamous flowers. International Journal of Plant Sciences, 163, 113-122. https://doi.org/10.1086/324180
  30. Damman, H., & Cain, M. L. (1998). Population growth and viability analyses of the clonal woodland herb, Asarum canadense. Journal of Ecology, 86, 13-26. https://doi.org/10.1046/j.1365-2745.1998.00242.x
  31. Eckert, C. G. (2002). The loss of sex in clonal plants. Evolutionary Ecology, 15, 501-520.
  32. Eriksson, O. (1985). Reproduction and clonal growth in Potentilla anserina L. (Rosaceae): the relation between growth form and dry weight allocation. Oecologia, 66, 378-380. https://doi.org/10.1007/BF00378302
  33. Eriksson, O. (1986). Survivorship, reproduction and dynamics of ramets of Potentilla anserina on a Baltic seashore meadow. Plant Ecology, 67, 17-25.
  34. Gara, B., & Muenchow, G. (1990). Chasmogamy/cleistogamy in Triodanis perfoliata (Campanulaceae): some CH/CL comparisons in fitness parameters. American Journal of Botany, 77, 1-6. https://doi.org/10.2307/2444786
  35. Gehring, J. L., & Linhart, Y. B. (1993). Sexual dimorphisms and response to low resources in the dioecious plant Silene latifolia (Caryophyllaceae). International Journal of Plant Sciences, 154, 152-162. https://doi.org/10.1086/297100
  36. Grace, J. B. (1993). The adaptive significance of clonal reproduction in angiosperms: an aquatic perspective. Aquatic Botany, 44, 159-180. https://doi.org/10.1016/0304-3770(93)90070-D
  37. Grant, V. (1981). Plant Speciation. New York: Columbia University Press.
  38. Handel, S. N. (1985). The intrusion of clonal growth patterns on plant breeding systems. American Naturalist, 125, 367-384. https://doi.org/10.1086/284348
  39. Harlan, J. R. (1945). Cleistogamy and chasmogamy in Bromus carinatus Hook. & Arn. American Journal of Botany, 32, 66-72. https://doi.org/10.2307/2437112
  40. Harper, J. L. (1977). Population biology of plants. San Diego: Academic Press.
  41. Husband, B. C., & Barrett, S. C. H. (1996). A metapopulation perspective in plant population biology. Journal of Ecology, 84, 461-469. https://doi.org/10.2307/2261207
  42. Hutchings, M. J. (1988). Differential foraging for resources and structural plasticity in plants. Trends in Ecology & Evolution, 3, 200-203. https://doi.org/10.1016/0169-5347(88)90007-9
  43. Ida, T. Y., & Kudo, G. (2009). Comparison of light harvesting and resource allocation strategies between two rhizomatous herbaceous species inhabiting deciduous forests. Journal of Plant Research, 122, 171-181. https://doi.org/10.1007/s10265-008-0212-6
  44. Jasienski, M., & Bazzaz, F. A. (1999). The fallacy of ratios and the testability of models in biology. Oikos, 84, 321-326. https://doi.org/10.2307/3546729
  45. Kaul, V., Koul, A. K., & Sharma, M. C. (2000). The underground flower. Current Science India, 78, 39-44.
  46. Kawano, S., Hara, T., Hiratsuka, A., Matsuo, K., & Hirota, I. (1990). Reproductive biology of an amphicarpic annual, Polygonum thunbergii (Polygonaceae): spatio-temporal changes in growth, structure and reproductive components of a population over an environmental gradient. Plant Species Biology, 5, 97-120. https://doi.org/10.1111/j.1442-1984.1990.tb00196.x
  47. Keeton, W. T. (1967). Biological science. New York: Norton and Co.
  48. Kim, J. H., Nam, J. M., & Kim, J. G. (2016). Effects of nutrient availability on the amphicarpic traits of Persicaria thunbergii. Aquatic Botany, 131, 45-50. https://doi.org/10.1016/j.aquabot.2016.03.001
  49. Kiviniemi, K. (2002). Population dynamics of Agrimonia eupatoria and Geum rivale, two perennial grassland species. Plant Ecology, 159, 153-169. https://doi.org/10.1023/A:1015506019670
  50. Klimes, L., Klimesova, J., Hendriks, R., & van Groenendael, J. (1997). Clonal plant architecture: a comparative analysis of form and function. In H. D. Kroon & J. V. Groenendael (Eds.), The ecology and evolution of clonal plants (pp. 1-29). Leiden: Backhuys Publishers.
  51. Koller, D., & Roth, N. (1964). Studies on the ecological and physiological significance of amphicarpy in Gymnarrhena micrantha (Compositae). American Journal of Botany, 51, 26-35. https://doi.org/10.2307/2440059
  52. Kozlowski, T. T. (1972). Seed Biology. New York: Academic Press.
  53. Kudoh, H., Shibaike, H., Takasu, H., Whigham, D. F., & Kawano, S. (1999). Genet structure and determinants of clonal structure in a temperate deciduous woodland herb, Uvularia perfoliata. Journal of Ecology, 87, 244-257. https://doi.org/10.1046/j.1365-2745.1999.00355.x
  54. Langer, R. H. M., & Wilson, D. (1965). Environmental control of cleistogamy in prairie grass (Bromus unioloides H.B.K.). New Phytologist, 64, 80-85. https://doi.org/10.1111/j.1469-8137.1965.tb05377.x
  55. Lei, S. A. (2010). Benefits and costs of vegetative and sexual reproduction in perennial plants: a review of literature. Journal of the Arizona-Nevada Academy of Science, 42, 9-14. https://doi.org/10.2181/036.042.0103
  56. Lenssen, J. P. M., Menting, F. B. J., Van Der Putten, W. H., & Blom, C. W. P. M. (2000). Vegetative reproduction by species with different adaptations to shallow-flooded habitats. New Phytologist, 145, 61-70. https://doi.org/10.1046/j.1469-8137.2000.00557.x
  57. Lenssen, J. P. M., Ten Dolle, G. E., & Blom, C. W. P. M. (1998). Flooding and the recruitment of reed marsh and tall forb plant species. Plant Ecology, 139, 13-23. https://doi.org/10.1023/A:1009754505028
  58. Li, B, Shibuya, T, Yogo, Y, Hara, T, Matsuo, K. (2001a). Effects of light quantity and quality on growth and reproduction of a clonal sedge, Cyperus esculentus. Plant Species Biology, 16, 69-81. https://doi.org/10.1046/j.1442-1984.2001.00049.x
  59. Li, BO, Shibuya, T, Yogo, Y, Hara, T, Yokozawa, M. (2001b). Interclonal differences, plasticity and trade-offs of life history traits of Cyperus esculentus in relation to water availability. Plant Species Biology, 16, 193-207. https://doi.org/10.1046/j.1442-1984.2001.00064.x
  60. Liu, F., Wu, W. Y., Wan, T., Wang, Q. F., Cheng, Y., & Li, W. (2013). Temporal variation of resource allocation between sexual and asexual structures in response to nutrient and water stress in a floating-leaved plant. Journal of Plant Ecology, 6, 499-505. https://doi.org/10.1093/jpe/rtt021
  61. Lloyd, D. G. (1984). Variation strategies in heterogeneous environments. Biological Journal of the Linnean Society, 21, 357-385. https://doi.org/10.1111/j.1095-8312.1984.tb01600.x
  62. Loehle, C. (1987). Partitioning of reproductive effort in clonal plants: a benefitcost model. Oikos, 49, 199-208. https://doi.org/10.2307/3566027
  63. Lopez-Almansa, J. C., Pannell, J. R., & Gil, L. (2003). Female sterility in Ulmus minor (Ulmaceae): a hypothesis invoking the cost of sex in a clonal plant. American Journal of Botany, 90, 603-609. https://doi.org/10.3732/ajb.90.4.603
  64. Lord, E. M. (1981). Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. Botanical Review, 47, 421-449. https://doi.org/10.1007/BF02860538
  65. Mal, T. K., & Lovett-Doust, J. (2005). Phenotypic plasticity in vegetative and reproductive traits in an invasive weed, Lythrum salicaria (Lythraceae), in response to soil moisture. American Journal of Botany, 92, 819-825. https://doi.org/10.3732/ajb.92.5.819
  66. Marino, P. C., Robert, M., Eisenberg, & Cornell, H. V. (1997). Influence of sunlight and soil nutrients on clonal growth and sexual reproduction of the understory perennial herb Sanguinaria canadensis L. The Journal of the Torrey Botanical Society, 124, 219-227. https://doi.org/10.2307/2996609
  67. Masuda, M., & Yahara, T. (1994). Reproductive ecology of a cleistogamous annual, Impatiens noli-tangere L., occurring under different environmental conditions. Ecological Research, 9, 67-75. https://doi.org/10.1007/BF02347243
  68. Maurer, D. A., & Zedler, J. B. (2002). Differential invasion of a wetland grass explained by tests of nutrients and light availability on establishment and clonal growth. Oecologia, 131, 279-288. https://doi.org/10.1007/s00442-002-0886-8
  69. Mccall, C., Mitchell-olds, T., & Waller, D. W. (1989). Fitness consequences of outcrossing in Impatiens capensis: tests of the frequency-dependent and sibcompetition models. Evolution, 43, 1075-1084.
  70. McNamara, J., & Quinn, J. A. (1977). Resource allocation and reproduction in populations of Amphicarpum purshii (Gramineae). American Journal of Botany, 64, 17-23. https://doi.org/10.2307/2441871
  71. Minter, T. C., & Lord, E. M. (1983). Effects of water stress, abscisic acid, and gibberellic acid on flower production and differentiation in the cleistogamous species Collomia grandiflora Dougl. Ex Lindl. (Polemoniaceae). American Journal of Botany, 70, 618-624. https://doi.org/10.2307/2443173
  72. Mitchell-olds, T., & Waller, D. M. (1985). Relative performance of selfed and outcrossed progeny in Impatiens capensis. Evolution, 39, 533-544. https://doi.org/10.1111/j.1558-5646.1985.tb00393.x
  73. Mony, C., Mercier, E., Bonis, A., & Bouzille, J. B. (2010). Reproductive strategies may explain plant tolerance to inundation: a mesocosm experiment using six marsh species. Aquatic Botany, 92, 99-104. https://doi.org/10.1016/j.aquabot.2009.10.011
  74. Morain, S. A. (1984). Systematic and regional biogeography. New York: Van Nostrand Reinhold Company.
  75. Motten, A. F. (1986). Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecological Monographs, 56, 21-42. https://doi.org/10.2307/2937269
  76. Nicholls, A. M. (2011). Size-dependent analysis of allocation to sexual and clonal reproduction in Penthorum sedoides under contrasting nutrient levels. International Journal of Plant Sciences, 172, 1077-1086. https://doi.org/10.1086/662128
  77. Nielsen, U. N., Riis, T., & Brix, H. (2006). The importance of vegetative and sexual dispersal of Luronium natans. Aquatic Botany, 84, 165-170. https://doi.org/10.1016/j.aquabot.2005.09.002
  78. Obeso, J. R. (2002). The costs of reproduction in plants. New Phytologist, 155, 321-348. https://doi.org/10.1046/j.1469-8137.2002.00477.x
  79. Ogden, J. (1974). The reproductive strategy of higher plants: II. The reproductive strategy of Tussilago Farfara L. Journal of Ecology, 62, 291-324. https://doi.org/10.2307/2258894
  80. Olivieri, I., Michalakis, Y., & Gouyon, P. H. (1995). Metapopulation genetics and the evolution of dispersal. American Naturalist, 164, 202-228.
  81. Philbrick, C. T., & Les, D. H. (1996). Evolution of aquatic angiosperm reproductive systems. Bioscience, 46, 813-26. https://doi.org/10.2307/1312967
  82. Piquot, Y., Petit, D., Valero, M., Cuguen, J., Laguerie, P. D., & Vernet, P. (1998). Variation in sexual and asexual reproduction among young and old populations of the perennial macrophyte Sparganium erectum. Oikos, 82, 139-148. https://doi.org/10.2307/3546924
  83. Pitelka, L. F., Stanton, D. S., & Peckenham, M. O. (1980). Effects of light and density on resource allocation in a forest herb, Aster acuminatus (Compositae). American Journal of Botany, 67, 942-948. https://doi.org/10.2307/2442435
  84. Pollux, B. J. A., Jong, M. D. E., Steegh, A., Verbruggen, E., Van Groenendael, J. M., & Ouborg, N. J. (2007). Reproductive strategy, clonal structure and genetic diversity in populations of the aquatic macrophyte Sparganium emersum in river systems. Molecular Ecology, 16, 313-325.
  85. Radosevich, S. R., Holt, J. S., & Ghersa, C. M. (1996). Weeds ecology: implications for management (2nd ed.). New York: John Wiley & Sons.
  86. Roff, D. A. (1992). The evolution of life histories. New York: Chapman and Hall.
  87. Ronsheim, M. L. (1996). Evidence against a frequency-dependent advantage for sexual reproduction in Allium vineale. American Naturalist, 147, 718-734. https://doi.org/10.1086/285876
  88. Ronsheim, M. L., & Bever, J. D. (2000). Genetic variation and evolutionary tradeoffs for sexual and asexual reproductive modes in Allium vineale (Liliaceae). American Journal of Botany, 87, 1769-1777. https://doi.org/10.2307/2656827
  89. Sadeh, A., Guterman, H., Gersani, M., & Ovadia, O. (2009). Plastic bet-hedging in an amphicarpic annual: an integrated strategy under variable conditions. Evolutionary Ecology, 23, 373-388. https://doi.org/10.1007/s10682-007-9232-2
  90. Sarukhan, J. (1974). Studies on plant demography: Ranunculus repens L., R. bulbosus L. and R. acris L. 2. Reproductive strategies and seed population dynamics. Journal of Ecology, 62, 151-177. https://doi.org/10.2307/2258886
  91. Schemske, D. W. (1978). Evolution of reproductive characteristics in Impatiens (Balsaminaceae): the significance of cleistogamy and chasmogamy. Ecology, 59, 596-613. https://doi.org/10.2307/1936588
  92. Schemske, D. W., Wilson, M. F., Melampy, M. N., Miller, L. J., Verner, L., Schemske, K. M., & Best, L. B. (1978). Flowering ecology of some spring woodland herbs. Ecology, 59, 351-366. https://doi.org/10.2307/1936379
  93. Schmitt, J., & Gamble, S. E. (1990). The effect of distance from the parental site on offspring performance and inbreeding depression in Impatiens capensis: a test of the local adaptation hypothesis. Evolution, 44, 2022-2030.
  94. Silvertown, J. (2008). The evolutionary maintenance of sexual reproduction: evidence from the ecological distribution of asexual reproduction in clonal plants. International Journal of Plant Sciences, 169, 157-168. https://doi.org/10.1086/523357
  95. Smith, RL, Smith, TM (2015). Elements of ecology. Global Edition, Pearson Education Limited.
  96. Stearns, S. C. (1989). Trade-offs in life history evolution. Functional Ecology, 3, 259-268. https://doi.org/10.2307/2389364
  97. Stebbins, G. L. (1974). Flowering plants: evolution above the species level. Cambridge: Belknap Press.
  98. Svenning, J. C. (2000). Growth strategies of clonal palms (Arecaceae) in a neotropical rainforest, Yasuni, Ecuador. Australian Journal of Botany, 48, 167-178. https://doi.org/10.1071/BT98048
  99. Thomas, A. G., & Dale, H. M. (1975). The role of seed reproduction in the dynamics of established populations of Hieracium floribundum and a comparison with that of vegetative reproduction. Canadian Journal of Botany, 53, 3022-3031. https://doi.org/10.1139/b75-331
  100. Thompson, F. L., & Eckert, C. G. (2004). Trade-offs between sexual and clonal reproduction in an aquatic plant: experimental manipulations vs. phenotypic correlations. Journal of evolutionary biology, 17, 581-592. https://doi.org/10.1111/j.1420-9101.2004.00701.x
  101. Tilman, D. (1988). Plant strategies and the dynamics and structure of plant communities. New York: Princeton Monographs.
  102. Trapp, E. J., & Hendrix, S. D. (1988). Consequences of a mixed reproductive system in the hog peanut, Amphicarpaea bracteata, (Fabaceae). Oecologia, 75, 285-290. https://doi.org/10.1007/BF00378611
  103. Turner, C. E. (1988). Ecology of invasions by weeds. In M. A. Altieri & M. Liebman (Eds.), Weed management in agroecosystem (pp. 41-55). Florida: Ecological Approaches CRC Press.
  104. van Andel, J., & Vera, F. (1977). Reproductive allocation in Senecio sylvaticus and Chamaenerion angustifolium in relation to mineral nutrition. Journal of Ecology, 65, 747-758. https://doi.org/10.2307/2259377
  105. van Breemen, N. (2013). Plant-induced soil changes: processes and feedbacks. Netherlands: Springer.
  106. van der Valk, A. G. (1981). Succession in wetlands: a gleasonian approach. Ecology, 62, 688-696. https://doi.org/10.2307/1937737
  107. van Kleunen, M., Fischer, M., & Schmid, B. (2002). Experimental life-history evolution: selection on the allocation to sexual reproduction and its plasticity in a clonal plant. Evolution, 56, 2168-2177. https://doi.org/10.1111/j.0014-3820.2002.tb00141.x
  108. Vange, V. (2002). Breeding system and inbreeding depression in the clonal plant species Knautia arvensis (Dipsacaceae): implications for survival in abandoned grassland. Biological Conservation, 108, 59-67. https://doi.org/10.1016/S0006-3207(02)00090-3
  109. Venable, D. L. (1985). The evolutionary ecology of seed heteromorphism. American Naturalist, 126, 577-595. https://doi.org/10.1086/284440
  110. Venable, D. L., & Brown, J. S. (1988). The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. American Naturalist, 131, 360-384. https://doi.org/10.1086/284795
  111. Venable, D. L., & Brown, J. S. (1993). The population-dynamic functions of seed dispersal. Vegetatio, 107, 31-55.
  112. Verburg, R. W., & During, H. J. (1998). Vegetative propagation and sexual reproduction in the woodland understorey pseudo-annual Circaea lutetiana L. Plant Ecology, 134, 211-224. https://doi.org/10.1023/A:1009741102627
  113. Walker, LR, Moral, R (2003). Primary succession and ecosystem rehabilitation. Hampshire: Cambridge University Press.
  114. Waller, D. M. (1980). Environmental determinants of outcrossing in Impatiens capensis (Balsaminaceae). Evolution, 34, 747-761. https://doi.org/10.1111/j.1558-5646.1980.tb04014.x
  115. Wang, M. T., Zhao, Z. G., Du, G. Z., & He, Y. L. (2008). Effects of light on the growth and clonal reproduction of Ligularia virgaurea. Journal of Integrative Plant Biology, 50, 1015-1023. https://doi.org/10.1111/j.1744-7909.2008.00645.x
  116. Wang, Y. J., Shi, X. P., & Zhong, Z. C. (2013). The relative importance of sexual reproduction and clonal propagation in rhizomatous herb Iris japonica Thunb. from two habitats of Jinyun Mountain, Southwest China. Russian Journal of Ecology, 44, 199-206. https://doi.org/10.1134/S106741361303017X
  117. Wang, Z., Xu, A., & Zhu, T. (2008). Plasticity in bud demography of a rhizomatous clonal plant Leymus chinensis L. in response to soil water status. Journal of Plant Biology, 51, 102-107. https://doi.org/10.1007/BF03030718
  118. Webster, T. M., & Grey, T. L. (2008). Growth and reproduction of Benghal dayflower (Commelina benghalensis) in response to drought stress. Weed Science, 56, 561-566. https://doi.org/10.1614/WS-07-186.1
  119. Weiss, P. W. (1980). Germination, reproduction and interference in the amphicarpic annual Emex spinosa (L.) Campd. Oecologia, 45, 244-251. https://doi.org/10.1007/BF00346465
  120. Whitefield, P (2009). The living landscape: how to read and understand it. Cambridge: Permanent Publications.
  121. Wilken, D. H. (1982). The balance between chasmogamy and cleistogamy in Collomia grandiflora (Polemoniaceae). American Journal of Botany, 69, 1326-1333. https://doi.org/10.2307/2442758
  122. Winkler, E., & Fischer, M. (2001). The role of vegetative and seed dispersal within habitats for optimal life histories of clonal plants: a simulation study. Evolutionary Ecology, 15, 281-301. https://doi.org/10.1023/A:1016080714200
  123. Worley, A. C., & Harder, L. D. (1996). Size-dependent resource allocation and costs of reproduction in Pinguicula vulgaris (Lentibulariaceae). Journal of Ecology, 84, 195-206. https://doi.org/10.2307/2261355
  124. Xiao, Y., Tang, J., Qing, H., Zhou, C., Kong, W., & An, S. (2011). Trade-offs among growth, clonal, and sexual reproduction in an invasive plant Spartina alterniflora responding to inundation and clonal integration. Hydrobiologia, 658, 353-363. https://doi.org/10.1007/s10750-010-0505-3
  125. Zhang, Y., & Zhang, D. (2007). Asexual and sexual reproductive strategies in clonal plants. Frontiers of Biology in China, 2, 256-262. https://doi.org/10.1007/s11515-007-0036-0

Cited by

  1. Establishment strategy of a rare wetland species Sparganium erectum in Korea vol.41, pp.8, 2016, https://doi.org/10.1186/s41610-017-0045-0
  2. Correction to: The optimal balance between sexual and asexual reproduction in variable environments: a systematic review vol.42, pp.1, 2016, https://doi.org/10.1186/s41610-018-0066-3
  3. Control of runner reed (Phragmites japonicus) in lentic wetlands vol.42, pp.4, 2016, https://doi.org/10.1186/s41610-018-0079-y
  4. Coevolution of the mitotic and meiotic modes of eukaryotic cellular division vol.98, pp.3, 2018, https://doi.org/10.1103/physreve.98.032409
  5. The clonal grass Leymus chinensis overcomes salt stress by over-compensatory growth of individual ramets vol.70, pp.11, 2019, https://doi.org/10.1071/cp18530
  6. Influence of die-back syndrome on reproductive strategies within Phragmites australis populations vol.153, pp.2, 2016, https://doi.org/10.1080/11263504.2018.1473302
  7. Changes in Reproductive Strategy of an Early Successional Species Penthorum chinense in Response to Nutrient and Moisture Levels vol.62, pp.2, 2016, https://doi.org/10.1007/s12374-018-0334-x
  8. Trifolium polymorphum: an amphicarpic species with an interesting reproductive biology vol.42, pp.4, 2019, https://doi.org/10.1007/s40415-019-00570-x
  9. Shade avoidance and reproductive strategies of an early successional species Penthorum chinense in relation to shade treatments vol.22, pp.3, 2020, https://doi.org/10.1111/plb.13086
  10. Nonlinear drought plasticity reveals intraspecific diversity in a dominant grass species vol.35, pp.2, 2016, https://doi.org/10.1111/1365-2435.13713
  11. Intensity and mode of Lindera melissifolia reproduction are affected by flooding and light availability vol.11, pp.19, 2016, https://doi.org/10.1002/ece3.8037
  12. Hybrid Form Pelophylax esculentus-ridibundus (Amphibia, Ranidae) from the Tisa River Drainage: Its Origin and Evolutionary Potential vol.55, pp.6, 2016, https://doi.org/10.3103/s0095452721060098
  13. Genetic diversity of common reed in the southern Baltic Sea region – Is there an influence of disturbance? vol.177, pp.None, 2016, https://doi.org/10.1016/j.aquabot.2021.103471