Biodiversity Science ›› 2018, Vol. 26 ›› Issue (5): 468-475.doi: 10.17520/biods.2018037

• Reviews • Previous Article     Next Article

Consequences of clonal growth on pollinator visitation in flowering plants

Hao Tian, Wanjin Liao*()   

  1. Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875
  • Received:2018-02-05 Accepted:2018-03-23 Online:2018-09-11
  • Liao Wanjin
  • About author:

    # Co-first authors

Clonal plants reproduce asexually via clonal growth and simultaneously reproduce sexually, and the consequences of clonal growth on pollination and mating have been one of the essential questions in ecology and evolution of plant reproduction. An increasing number of studies report the effects of clonal size, architecture, genetic diversity, and floral deployments on pollinator visit and behavior. The most common view is that clonal growth produces large floral displays and therefore increases attraction to pollinators. Consequently, clonal growth may help to maximize male reproductive success by dispersing more pollen. On the other hand, geitonogamy, pollination among flowers within one individual plant, is an inevitable byproduct with an increase in clone size. More frequent geitonogamous pollination has been expected in clonal plants with large floral displays and leads to a reduction in female fitness because of inbreeding depression or pollen clogging. However, some recent theoretical and empirical studies suggest new ideas on this issue. First, the number of flowers visited by individual pollinator within a clone did not increase proportionally with clone size in clumped clonal plants, and pollinator movements within a single bout mainly occurred within ramet. The selfing component analyses based on molecular markers further evidenced that within-ramet geitonogamy was the largest contributing factor to the total geitonogamy in two clonal species. Second, the experimental study of bumblebees foraging on artificial flowers showed that when the same amount of flowers was distributed among multiple ramets, geitonogamy was not higher but in fact, lower compared with one single inflorescence. The model-based simulation suggested clonal growth could promote pollination quality without increasing geitonogamy when flowers simultaneously received and donated pollen. These studies support a novel explanation of the evolution of clonality in plants. Future studies on the pollination ecology of clonal plants may focus on the effects of clonal growth on pollinator behavior and plant mating from multiple angles. Comparative studies between clonal and non-clonal taxa or between clonal and non-clonal populations of the same species are required to evaluate the ecological and evolutionary consequences of clonal growth.

Key words: clonal architecture, clonal growth, floral deployments, geitonogamous pollination, mating system, pollinator behavior

1 Ackerman JD (2000) Abiotic pollen and pollination: Ecological, functional, and evolutionary perspectives. Plant Systematics and Evolution, 222, 167-185.
2 Aizen MA (1993) Self-pollination shortens flower lifespan in Portulaca umbraticola H. B. K. (Portulacaceae). International Journal of Plant Sciences, 154, 412-415.
3 Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: Effects of pollen quantity and quality. Ecology, 88, 271-281.
4 Albert T, Raspé O, Jacquemart AL (2008) Influence of clonal growth on selfing rate in Vaccinium myrtillus L. Plant Biology, 10, 643-649.
5 Baker HG (1963) Evolutionary mechanisms in pollination biology: Origins and functions of floral systems are being elucidated by genetical and ecological studies. Science, 139, 877-883.
6 Barrett SCH (2002) Sexual interference of the floral kind. Heredity, 88, 154-159.
7 Barrett SCH (2015) Influences of clonality on plant sexual reproduction. Proceedings of the National Academy of Sciences, USA, 112, 8859-8866.
8 Barrett SCH, Harder LD (1996) Ecology and evolution of plant mating. Trends in Ecology and Evolution, 11, 73-79.
9 Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genetics Research, 70, 155-174.
10 Charlesworth D, Charlesworth B (1995) Quantitative genetics in plants: The effect of breeding system on genetic variability. Evolution, 49, 911-920.
11 Charpentier A (2002) Consequences of clonal growth for plant mating. Evolutionary Ecology, 15, 521-530.
12 Cox PA (1993) Water-pollinated plants. Scientific American, 269, 68-74.
13 Darwin CR (1862) The Various Contrivances by Which Orchids Are Fertilized by Insects. John Murray, London.
14 Darwin CR (1877) The Different Forms of Flowers on Plants of the Same Species. John Murray, London.
15 de Jong TJ, Waser NM, Klinkhamer PGL (1993) Geitonogamy: The neglected side of selfing. Trends in Ecology and Evolution, 8, 321-325.
16 Dodd SC (1997) Genetic diversity in Delphinium variegatum (Ranunculaceae): A comparison of two island endemic subspecies and their widespread mainland relative. American Journal of Botany, 89, 613-622.
17 Eckert CG (2000) Contributions of autogamy and geitonogamy to self-fertilization in a mass-flowering, clonal plant. Ecology, 81, 532-542.
18 Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics, 35, 375-403.
19 Genung MA, Lessard JP, Brown CB, Bunn WA, Cregger MA, Reynolds WN, Quinn EF, Stevenson ML, Hartley AS, Crutsinger GM, Schweitzer JA, Bailey JK (2010) Non-additive effects of genotypic diversity increase floral abundance and abundance of floral visitors. PLoS ONE, 5, e8711.
20 Ghazoul J (2006) Floral diversity and the facilitation of pollination. Journal of Ecology, 94, 295-304.
21 Gonzalez-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyorgyi H, Woyciechowski M, Vila M (2013) Combined effects of global change pressures on animal-mediated pollination. Trends in Ecology and Evolution, 28, 524-530.
22 Hafdahl CE, Craig TP (2014) Flowering phenology in Solidago altissima: Adaptive strategies against temporal variation in temperature. Journal of Plant Interactions, 9, 122-127.
23 Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society: Biological Sciences, 351, 1291-1298.
24 Handel SN (1985) The intrusion of clonal growth patterns on plant breeding systems. The American Naturalist, 125, 367-384.
25 Hao YQ, Zhao XF, She DY, Xu B, Zhang DY, Liao WJ (2012) The role of late-acting self-incompatibility and early-acting inbreeding depression in governing female fertility in monkshood, Aconitum kusnezoffii. PLoS ONE, 7, e47034.
26 Harder LD, Barrett SCH, Cole WW (2000) The mating consequences of sexual segregation within inflorescences of flowering plants. Proceedings of the Royal Society B: Biological Sciences, 267, 315-320.
27 Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature, 373, 512-515.
28 Harder LD, Johnson SD (2005) Adaptive plasticity of floral display size in animal-pollinated plant. Proceedings of the Royal Society B: Biological Sciences, 272, 2651-2657.
29 Harder LD, Jordan CY, Gross WE, Routley MB (2004) Beyond floricentrism: The pollination function of inflorescences. Plant Species Biology, 19, 137-148.
30 Hu Y, Barrett SCH, Zhang DY, Liao WJ (2015) Experimental analysis of mating patterns in a clonal plant reveals contrasting modes of self-pollination. Ecology and Evolution, 5, 5423-5431.
31 Huang SQ, Guo YH (2000) Advances in the studies of pollination biology. Chinese Science Bulletin, 45, 225-237.
32 Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution, 50, 54-70.
33 Ishii HS, Hirabayashi Y, Kudo G (2008) Combined effects of inflorescence architecture, display size, plant density and empty flowers on bumble bee behaviour: Experimental study with artificial inflorescences. Oecologia, 156, 341-350.
34 Ito E, Kikuzawa K (2003) Reduction of geitonogamy: Flower abscission for departure of pollinators. Ecological Research, 18, 177-183.
35 Iwata T, Nagasaki O, Ishii HS, Ushimaru A (2012) Inflorescence architecture affects pollinator behaviour and mating success in Spiranthes sinensis (Orchidaceae). New Phytologist, 193, 196-203.
36 Jain SK (1976) The evolution of inbreeding in plants. Annual Review of Ecology and Systematics, 7, 469-495.
37 Jersáková J, Johnson SD (2006) Lack of floral nectar reduces self-pollination in a fly-pollinated orchid. Oecologia, 147, 60-68.
38 Jordan CY, Harder LD (2006) Manipulation of bee behavior by inflorescence architecture and its consequences for plant mating. The American Naturalist, 167, 496-509.
39 Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: An explanation for the biodiversity and ecosystem functioning relationship. Ecology, 87, 1244-1255.
40 Karron JD, Mitchell RJ (2012) Effects of floral display size on male and female reproductive success in Mimulus ringens. Annals of Botany, 109, 563-570.
41 Kevan PG (1990) How large bees, Bombus and Xylocopa (Apoidea Hymenoptera) forage on trees: Optimality and patterns of movement in temperate and tropical climates. Ethology Ecology & Evolution, 2, 233-242.
42 Klimeš L, Klimešová J, Hendriks R, Groenendael JV (1997) Clonal plant architecture: A comparative analysis of form and function. In: The Ecology and Evolution of Clonal Plants (eds de Kroon H, van Groenendael J), pp. 1-29. Backhuys Publishers, Leiden.
43 Klinkhamer PGL, de Jong T (1993) Attractiveness to pollinators: A plant’s dilemma. Oikos, 66, 180-184.
44 Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T (2005) Pollen limitation of plant reproduction: Pattern and process. Annual Review of Ecology, Evolution, and Systematics, 36, 467-497.
45 Li XM, She DY, Zhang DY, Liao WJ (2015) Life history trait differentiation and local adaptation in invasive populations of Ambrosia artemisiifolia in China. Oecologia, 177, 669-677.
46 Liao WJ, Harder LD (2014) Consequences of multiple inflorescences and clonality for pollinator behavior and plant mating. The American Naturalist, 184, 580-592.
47 Liao WJ, Hu Y, Zhu BR, Zhao XQ, Zeng YF, Zhang DY (2009) Female reproductive success decreases with display size in monkshood, Aconitum kusnezoffii (Ranunculaceae). Annals of Botany, 104, 1405-1412.
48 Lovett-Doust L (1981) Population dynamics and local specialization in a clonal perennial (Ranunculus repens). I. The dynamic of ramets in contrasting habitats. Journal of Ecology, 69, 743-755.
49 Ma HP, Zhao DH, Liao WJ (2012) Flight patterns of bumblebees (Bombus ignitus) on vertical inflorescences of Aconitum kusnezoffii. Biodiversity Science, 20, 405-408. (in Chinese with English abstract)
[马海萍, 赵大贺, 廖万金 (2012) 草乌花蜜产量的梯度分布及熊蜂自下而上的访花行为. 生物多样性, 20, 405-408.]
50 Mori Y, Nagamitsu T, Kubo T (2009) Clonal growth and its effects on male and female reproductive success in Prunus ssiori (Rosaceae). Population Ecology, 51, 175-186.
51 Nuortila C, Tuomi J, Laine K (2002) Inter-parent distance affects reproductive success in two clonal dwarf shrubs, Vaccinium myrtillus and Vaccinium vitis-idaea (Ericaceae). Canadian Journal of Botany, 80, 875-884.
52 Ohashi K, Yahara T (1998) Effects of variation in flower number on pollinator visits in Cirsium purpuratum (Asteraceae). American Journal of Botany, 85, 219-224.
53 Ohashi K, Yahara T (2002) Visit larger displays but probe proportionally fewer flowers: Counterintuitive behaviour of nectar-collecting bumble bees achieves an ideal free distribution. Functional Ecology, 16, 492-503.
54 Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos, 120, 321-326.
55 Pan JJ, Price JS (2001) Fitness and evolution in clonal plants: The impact of clonal growth. Evolutionary Ecology, 15, 583-600.
56 Peakall R, Beattie AJ (1991) The genetic consequences of worker ant pollination in a self-compatible, clonal orchid. Evolution, 45, 1837-1848.
57 Porcher E, Lande R (2005) The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. Journal of Evolutionary Biology, 18, 497-508.
58 Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: Trends, impacts and drivers. Trends in Ecology and Evolution, 25, 345-353.
59 Pyke GH (1978) Optimal foraging in bumblebees and coevolution with their plants. Oecologia, 36, 281-293.
60 Richter TS, Soltis PS, Soltis DE (1994) Genetic variation within and among populations of the narrow endemic, Delphinium viridescens (Ranunculaceae). American Journal of Botany, 81, 1070-1076.
61 Rosas-Guerrero V, Aguilar R, Marten-Rodriguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: Do floral traits predict effective pollinators? Ecology Letters, 17, 388-400.
62 Routley MB, Kron P, Husband BC (2004) The consequences of clone size for paternal and maternal success in domestic apple (Malus × domestica). American Journal of Botany, 91, 1326-1332.
63 Sage TL, Strumas F, Cole WW, Barrett SCH (1999) Differential ovule development following self- and cross-pollination: The basis of self-sterility in Narcissus triandrus (Amaryllidaceae). American Journal of Botany, 86, 855-870.
64 Schoen DL, Brown AHD (1991) Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proceedings of the National Academy of Sciences, USA, 88, 4494-4497.
65 Snow AA, Spira TP, Simpson R, Klips RA (1996) The ecology of geitonogamous pollination. In: Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (eds Lloyd DG, Barrett SCH), pp. 191-216. Chapman and Hall, New York.
66 Stebbins GL (1950) Variation and Evolution in Plants. Oxford University Press, London.
67 Tarasjev A (2005) Impact of genet size and flowering stage on fruit set in Iris pumila L. clones in wild. Acta Oecologica, 27, 93-98.
68 Vallejo-Marín M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annual Review of Ecology, Evolution, and Systematics, 41, 193-213.
69 van Drunen WE, van Kleunen M, Dorken ME (2015) Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal. Proceedings of the National Academy of Sciences, USA, 112, 8929-8936.
70 Vaughton G, Ramsey M (2010) Pollinator-mediated selfing erodes the flexibility of the best-of-both-worlds mating strategy in Bulbine vagans. Functional Ecology, 24, 374-382.
71 Waser NM, Ollerton J (2006) Plant-Pollinator Interactions From Specialization to Generalization. University of Chicago Press, Chicago.
72 Werner PA, Bradbury IK, Gross RS (1980) The biology of Canadian weeds. 45. Solidago canadensis L. Canadian Journal of Plant Science, 60, 1393-1409.
73 Williams CF, Ruvinsky J, Scott PE, Hews DK (2001) Pollination, breeding system, and genetic structure in two sympatric Delphinium (Ranunculaceae) species. American Journal of Botany, 88, 1623-1633.
74 Zhang DY, Jiang XH (2001) Mating system evolution, resource allocation, and genetic diversity in plants. Acta Phytoecologica Sinica, 25, 130-143. (in Chinese with English abstract)
[张大勇, 姜新华 (2001) 植物交配系统的进化、资源分配对策与遗传多样性. 植物生态学报, 25, 130-143.]
75 Zhang YF, Zhang DY (2006) Asexual and sexual reproductive strategies in clonal plants. Acta Phytoecologica Sinica, 30, 174-183. (in Chinese with English abstract)
[张玉芬, 张大勇 (2006) 克隆植物的无性与有性繁殖对策. 植物生态学报, 30, 174-183.]
[1] ZHANG Xin-Xin, WANG Xi, HU Ying, ZHOU Wei, CHEN Xiao-Yang, HU Xin-Sheng. (2019) Advances in the study of population genetic diversity at plant species’ margins . Chin J Plant Ecol, 43(5): 383-395.
[2] Lei Li,Yupeng Geng,Zhichun Lan,Jiakuan Chen,Zhiping Song. (2016) Phenotypic plasticity of aquatic plants in heterogeneous environments: a review . Biodiv Sci, 24(2): 216-227.
[3] Wei Ning, Jian Zhang, Zhigang Wu, Ming Ma, Xin Zhao, Tianlai Li. (2014) Characteristics of Obligate Apomixis in Dandelion (Taraxacum antungense) . Chin Bull Bot, 49(4): 417-423.
[4] Guanglu Liu, Shaohui Fan, Chunju Cai, Dapeng Zhang. (2013) Comparative Analysis on the Clonal Growth Characteristics of Bambusa pervariabilis × Dendrocalamopsis daii and B. rigida . Chin Bull Bot, 48(3): 288-294.
[5] GE Jun and XING Fu. (2012) A review of adaptive strategies of clonal plants to interspecific competition . Chin J Plan Ecolo, 36(6): 587-596.
[6] Xia Wang, Jing Wang, Jinghu Jiang, Ming Kang. (2012) Genetic diversity and the mating system in a fragmented population of Tsoongiodendron odorum . Biodiv Sci, 20(6): 676-684.
[7] Zhijun Li, Peipei Jiao, Zhengli Zhou, Qian Li, Jianqiang Li. (2012) Morphological and Anatomical Features of Root Sucker Propagation of Populus pruinosa . Chin Bull Bot, 47(2): 133-140.
[8] Xin Jia, Xingzhong Yang, Xiaoyun Pan, Bo Li, Jiakuan Chen. (2008) Vegetative propagation characteristics of Alternanthera philoxeroides in response to disturbances . Biodiv Sci, 16(3): 229-235.
[9] Lulu Tang, Bing Han. (2007) Effects of floral display on pollinator behavior and pollen dispersal . Biodiv Sci, 15(6): 680-686.
[11] WEI Xiao-Hui, YIN Dong-Sheng, ZHU Ning. (2007) CLONAL ARCHITECTURE OF PHYSOCARPUS AMURENSISIN NATURAL CONDITIONS . Chin J Plan Ecolo, 31(4): 625-629.
[15] Liqin Pan, Hua Ji, Longqing Chen. (2005) Genetic diversity of the natural populations of Adiantum reniforme var. sinense . Biodiv Sci, 13(2): 122-129.
Full text