Phenotypic plasticity of aquatic plants in heterogeneous environments: a review

doi:10.17520/biods.2015214

Abstract

Abstract:

Aquatic plants are the ecological group that mainly consists of herbaceous plants with habitats that are closely associated with water. Most aquatic plants have strong clonality. In response to changes in aquatic environments, aquatic plants exhibit significant plasticity in morphological, behavioral and physiological traits, and thus adapt well to heterogeneous aquatic environments. Compared with extensive studies on phenotypic plasticity of terrestrial plants, less attention has been paid to test how phenotypic plasticity of aquatic plants responds to heterogeneous environments. In this review, we briefly clarified the major types of phenotypic plasticity and their relationships in clonal plants in heterogeneous environments, identified the uniqueness of aquatic environments in relation to environmental heterogeneity, and analyzed the theoretical possibilities of aquatic plants showing high phenotypic plasticity. Furthermore, we probed into how aquatic plants adapted to heterogeneous aquatic environments by means of phenotypic plasticity involved with morphological plasticity, foraging behavior, clonal integration, intraclonal labour division, and risk spreading. Finally, we identified shortcomings in current studies on phenotypic plasticity of aquatic plants, and highlighted some issues deserving more attention in future studies, which include: (1) the changing pattern and mechanism of phenotypic plasticity; (2) the influence of clonal integration on community and ecosystem stability; (3) the trade-offs between clonal integration and fragmentation; (4) the differences of phenotypic plasticity in different types of clonal architecture, and their mechanisms; (5) the adaptive evolution of phenotypic plasticity; (6) the interaction of aquatic plants with species in other taxa or at different tropic levels; and (7) the response of aquatic ecosystems to global change.

Key words: environmental heterogeneity, aquatic plant, clonal growth, morphological plasticity, clonal integration, foraging behavior, intraclonal labour division, risk spreading

Lei Li, Yupeng Geng, Zhichun Lan, Jiakuan Chen, Zhiping Song. Phenotypic plasticity of aquatic plants in heterogeneous environments: a review[J]. Biodiv Sci, 2016, 24(2): 216-227.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2015214

https://www.biodiversity-science.net/EN/Y2016/V24/I2/216

References 112

1	Barrett SCH, Echert CG, Husband BC (1993) Evolutionary processes in aquatic plant populations. Aquatic Botany, 44, 105-145.
2	Boeger MRT, Poulson ME (2003) Morphological adaptations and photosynthetic rates of amphibious Veronica anagallis-aquatica L. (Scrophulariaceae) under different flow regimes. Aquatic Botany, 75, 123-135.
3	Bornette G, Puijalon S (2011) Response of aquatic plants to abiotic factors: a review. Aquatic Sciences, 73, 1-14.
4	Chambers PA, Lacoul P, Murphy KJ, Thomaz SM (2008) Global diversity of aquatic macrophytes in freshwater. Hydrobiologia, 595, 9-26.
5	Chambers PA, Prepas EE (1988) Underwater spectral attenuation and its effect on the maximum depth of angiosperm colonization. Canadian Journal of Fish Aquatic Science, 45, 1010-1017.
6	Chappuis E, Gacia E, Ballesteros E (2014) Environmental factors explaining the distribution and diversity of vascular aquatic macrophytes in a highly heterogeneous Mediterranean region. Aquatic Botany, 113, 72-82.
7	Chen YD (2011) The Chinese Aquatic Plants. Henan Science and Technology Press, Zhengzhou. (in Chinese)
	[陈耀东 (2011) 中国水生植物. 河南科学技术出版社, 郑州.]
8	Chen YF, Yu FH, Dong M (2002) Scale-dependent spatial heterogeneity of vegetation in Mu Us sandy land in semi-arid area of China. Plant Ecology, 162, 135-142.
9	Cook CDK (1999) The number and kinds of embryo-bearing plants which have become aquatic. Perspectives in Plant Ecology, Evolution and Systematics, 2, 79-102.
10	Cook RE (1985) Growth and development in clonal plant population. In: Population Biology and Evolution of Clonal Organism (ed Jackson JBC, Buss LW, Cook RE), pp. 259-296. Yale University Press, New Haven.
11	Cronk JK, Fennessy MS (2001) Wetland Plants: Biology and Ecology. CRC Press, Florida.
12	Cushing CE, Allan JD (2001) Streams: Their Ecology and Life. Academic Press, San Diego.
13	de Kroons H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytologist, 166, 73-82.
14	de Kroons H, Hutchings MJ (1995) Morphological plasticity in clonal plants: the foraging concept reconsidered. Journal of Ecology, 83, 143-152.
15	De Wilde M, Sebei N, Puijalon S, Bornette G (2014) Responses of macrophytes to dewatering: effects of phylogeny and phenotypic plasticity on species performance. Evolutionary Ecology, 2014, 28, 1155-1167.
16	D’Hertefeldt T, van der Putten WH (1998) Physiological integration of the clonal plant Carex arenaria and its response to soil-borne pathogens. Oikos, 81, 229-237.
17	Dong BC, Alpert P, Guo W, Yu FH (2012) Effects of fragmentation on the survival and growth of the invasive, clonal plant Alternanthera philoxeroides. Biological Invasions, 14, 1101-1110.
18	Dong BC, Yu GL, Guo W, Zhang MX, Dong M, Yu FH (2010) How internode length, position and presence of leaves affect survival and growth of Alternanthera philoxeroides after fragmentation? Evolutionary Ecology, 24, 1447-1461.
19	Dong M (1996a) Clonal growth in plants in relation to resource heterogeneity: foraging behavior. Acta Botanica Sinica, 38, 828-835. (in Chinese with English abstract)
	[董鸣 (1996a) 资源异质环境中的植物克隆生长: 觅食行为. 植物学报, 38, 828-835.]
20	Dong M (1996b) Plant clonal growth in heterogeneous habitats: risk-spreading. Acta Phytoecologica Sinica, 20, 543-548. (in Chinese with English abstract)
	[董鸣 (1996b) 异质性生境中的植物克隆生长: 风险分摊. 植物生态学报, 20, 543-548.]
21	Dong M (2011) Clonal Plant Ecology. Science Press, Beijing.
	(in Chinese) [董鸣 (2011) 克隆植物生态学科学出版社, 北京.]
22	Duarte CM, Kalff J (1988) Influence of lake morphometry on the response of submerged macrophytes to sediment fertilization. Canadian Journal of Fish Aquatic Science, 45, 216-221.
23	Duarte CM, Kalff J, Peters RH (1986) Patterns in biomass and cover of aquatic macrophytes in lakes. Canadian Journal of Fish Aquatic Science, 43, 1900-1908.
24	Elgersma KJ, Wildová R, Martina JP, Currie WS, Goldberg DE (2015) Does clonal resource translocation relate to invasiveness of Typha taxa? Results from a common garden experiment. Aquatic Botany, 126, 48-53.
25	Fleming JP, Dibble ED (2015) Ecological mechanisms of invasion success in aquatic macrophytes. Hydrobiologia, 746, 23-37.
26	Fu H, Yuan GX, Cao T, Ni LY, Zhang M, Wang SR (2012) An alternative mechanism for shade adaptation: implication of allometric responses of three submersed macrophytes to water depth. Ecological Research, 27, 1087-1094.
27	Ganie AH, Reshi ZA, Wafai BA, Puijalon S (2015) Phenotypic plasticity: cause of the successful spread of the genus Potamogeton in the Kashmir Himalaya. Aquatic Botany, 120, 283-289.
28	Gantes HP, Caro AS (2001) Environmental heterogeneity and spatial distribution of macrophytes in plain streams. Aquatic Botany, 70, 225-236.
29	Gao L, Li B, Liu WY, Shen YX, Liu WJ (2013) Inhibition effects of daughter ramets on parent of clonal plant Eichhornia crassipes. Aquatic Botany, 107, 47-53.
30	Geng YP, Pan XY, Xu CY, Zhang WJ, Li B, Chen JK, Lu BR, Song ZP (2007) Phenotypic plasticity rather than locally adapted ecotypes allows the invasive alligator weed to colonize a wide range of habitats. Biological Invasions, 9, 245-256.
31	Geng YP, Zhang WJ, Li B, Chen JK (2004) Phenotypic plasticity and invasiveness of alien plants. Biodiversity Science, 12, 447-455. (in Chinese with English abstract)
	[耿宇鹏, 张文驹, 李博, 陈家宽 (2004) 表型可塑性与外来植物的入侵能力. 生物多样性, 12, 447-455.]
32	Gómez S, Onoda Y, Ossipov V, Stuefer JF (2008) Systemic induced resistance: a risk-spreading strategy in clonal plant networks? New Phytologist, 179, 1142-1153.
33	Grace JB (1993) The adaptive significance of clonal reproduction in angiosperms: an aquatic perspective. Aquatic Botany, 44, 159-180.
34	Guo YH, Huang SQ, Chen JK (1998) Breeding system and evolution of aquatic angiosperms. Acta Hydrobiologica Sinica, 22, 79-85. (in Chinese with English abstract)
	[郭友好, 黄双全, 陈家宽 (1998) 水生被子植物的繁育系统与进化. 水生生物学报, 22, 79-85.]
35	Herben T (2004) Physiological integration affects growth form and competitive ability in clonal plants. Evolutionary Ecology, 18, 493-520.
36	Holmes MG, Klein WH (1987) The light and temperature environments. In: Plant Life in Aquatic and Amphibious Habitats (ed. Crawford RMM), pp. 3-22. Blackwell, Oxford.
37	Hussner A, Meyer C, Busch J (2009) The influence of water level and nutrient availability on growth and root system development of Myriophyllum aquaticum. Weed Research, 49, 73-80.
38	Hutchings MJ, Wijesinghe DK (1997) Patchy habitats, division of labor and growth dividends in clonal plants. Trends in Ecology & Evolution, 12, 390-394.
39	Hyldgaard B, Brix H (2012) Intraspecies differences in phenotypic plasticity: invasive versus non-invasive populations of Ceratophyllum demersum. Aquatic Botany, 97, 49-56.
40	Ikegami M, van Hal S, van Rheenen JW, Whigham DF, Werger MJ (2008) Spatial division of labour of Schoenoplectus americanus. Plant Ecology, 199, 55-64.
41	Jackson RB, Caldwell MM (1993) The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics. Ecology, 74, 612-614.
42	Jensen S, Bell S (2001) Seagrass growth and patch dynamics: cross-scale morphological plasticity. Plant Ecology, 155, 201-217.
43	Kotschy K, Rogers K (2008) Reed clonal characteristics and response to disturbance in a semi-arid river. Aquatic Botany, 88, 47-56.
44	Květ J, Westlake S, Dykyjová D, Marshall EJP, Ondok JP (1988) Primary production in wetlands. In: The Production Ecology of Wetlands: The IBP Synthesis (ed Westlake DF, Květ J, Szczepański A), pp. 78-169. Cambridge University Press, Cambridge.
45	Lacoul P, Freedman B (2006) Environmental influences on aquatic plants in freshwater ecosystems. Environmental Reviews, 14, 89-136.
46	Li HL, Xu YS, Wang YY, Yu NQ, Zhang MX, Lei GC, Yu FH (2015) Does clonal fragmentation of the floating plant Eichhornia crassipes affect the growth of submerged macrophyte communities?. Folia Geobotanica, 2015, 50, 283-291.
47	Liao MJ, Yu FH, Song MH, Zhang SM, Zhang JZ, Dong M (2003) Plasticity in R/S ratio, morphology and fitness- related traits in response to reciprocal patchiness of light and nutrients in the stoloniferous herb, Glechoma longituba. Acta Oecologica, 24, 231-239.
48	Luo FL, Chen Y, Huang L, Wang A, Zhang MX, Yu FH (2014) Shifting effects of physiological integration on performance of a clonal plant during submergence and de-submergence. Annals of Botany, 113, 1265-1274.
49	Luo WB, Xie YH, Song FB (2007) Survival strategies of wetland plants in flooding environments. Chinese Journal of Ecology, 26, 1478-1485. (in Chinese with English abstract)
	[罗文泊, 谢永宏, 宋凤斌 (2007) 洪水条件下湿地植物的生存策略. 生态学杂志, 26, 1478-1485.]
50	Maberly SC, Spence DHN (1983) Photosynthetic inorganic carbon use by freshwater plants. Journal of Ecology, 71, 705-724.
51	Mal TK, 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.
52	Marbà N, Hemminga MA, Mateo MA, Duarte CM, Maas YEM, Terrados J, Gacia E (2002) Carbon and nitrogen translocation between seagrass ramets. Marine Ecology Progress Series, 226, 287-300.
53	Marshall C (1990) Source-sink relations of interconnecte ramets. In: Clonal Growth in Plants: Regulations and Functions (eds van Groenendael J, de Kroon H), pp. 23-41. SPB Academic Publishing, Hague.
54	Middelboe AL, Markager S (1997) Depth limits and minimum light requirements of freshwater macrophytes. Freshwater Biology, 37, 553-568.
55	Middleton BA, van der Valk AG, Davis CB (2015) Responses to water depth and clipping of twenty-three plant species in an Indian monsoonal wetland. Aquatic Botany, 126, 38-47.
56	Okada M, Grewell BJ, Jasieniuk M (2009) Clonal spread of invasive Ludwigia hexapetala and L. grandiflora in freshwater wetlands of California. Aquatic Botany, 91, 123-129.
57	Ooi JLS, Kendrick GA, van Niel KP (2011) Effects of sediment burial on tropical ruderal seagrasses are moderated by clonal integration. Continental Shelf Research, 31, 1945-1954.
58	Peltzer DA (2002) Does clonal integration improve competitive ability? A test using aspen (Populus tremuloides [Salicaceae]) invasion into prairie. American Journal of Botany, 89, 494-499.
59	Peterson AG, Chesson P (2002) Short-term fitness benefits of physiological integration in the clonal herb Hydrocotyle peduncularis. Austral Ecology, 27, 647-657.
60	Philbrick CT, Les DH (1996) Evolution of aquatic angiosperm reproductive systems: What is the balance between sexual and asexual reproduction in aquatic angiosperms? BioScience, 46, 813-826.
61	Pinno BD, Wilson SD (2014) Nitrogen translocation between clonal mother and daughter trees at a grassland-forest boundary. Plant Ecology, 215, 347-354.
62	Puijalon S, Bornette G (2006) Phenotypic plasticity and mechanical stress: biomass partitioning and clonal growth of an aquatic plant species. American Journal of Botany, 93, 1090-1099.
63	Puijalon S, Bouma TJ, Van Groenendael J, Bornette G (2008a) Clonal plasticity of aquatic plant species submitted to mechanical stress: escape versus resistance strategy. Annals of Botany, 102, 989-996.
64	Puijalon S, Léna JP, Rivière N, Champagne JY, Rostan JC, Bornette G (2008b) Phenotypic plasticity in response to mechanical stress: hydrodynamic performance and fitness of four aquatic plant species. New Phytologist, 177, 907-917.
65	Riis T, Lambertini C, Olesen B, Clayton JS, Brix H, Sorrell BK (2010) Invasion strategies in clonal aquatic plants: Are phenotypic differences caused by phenotypic plasticity or local adaptation? Annals of Botany, 106, 813-822.
66	Riis T, Olesen B, Clayton JS, Lambertini C, Brix H, Sorrell BK (2012) Growth and morphology in relation to temperature and light availability during the establishment of three invasive aquatic plant species. Aquatic Botany, 102, 56-64.
67	Roiloa SR, Alpert P, Tharayil N, Hancock G, Bhowmik PC (2007) Greater capacity for division of labour in clones of Fragaria chiloensis from patchier habitats. Journal of Ecology, 95, 397-405.
68	Santamaría L (2002) Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecologica, 23, 137-154.
69	Santamaría L, Montes C, Hootsmans MJM (1996) Influence of environmental parameters on the biomass development of Ruppia drepanensis populations in Doñana National Park: the importance of conditions affecting the underwater light climate. International Journal of Salt Lake Research, 5, 157-180.
70	Schmidt BL, Millington WF (1968) Regulation of leaf shape in Proserpinaca palustris. Bulletin of the Torrey Botanical Club, 95, 264-286.
71	Song YB, Yu FH, Keser LH, Dawson W, Fischer M, Dong M, van Kleunen M (2013) United we stand, divided we fall: a meta-analysis of experiments on clonal integration and its relationship to invasiveness. Oecologia, 171, 317-327.
72	Spencer WE, Teeri J, Wetzel RG (1994) Acclimation of photosynthetic phenotype to environmental heterogeneity. Ecology, 75, 301-314.
73	Strand JA, Weisner SE (2001) Morphological plastic responses to water depth and wave exposure in an aquatic plant (Myriophyllum spicatum). Journal of Ecology, 89, 166-175.
74	Stuefer JF, de Kroon H, During HJ (1996) Exploitation of environmental heterogeneity by spatial division of labour in a clonal plant. Functional Ecology, 10, 328-334.
75	Stuefer JF, Gómez S, van Mölken T (2004) Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks. Evolutionary Ecology, 18, 647-667.
76	Tang JB, Xiao Y, An SQ (2010) Advance of studies on rhizomatous clonal plant ecology. Acta Ecologica Sinica, 30, 3028-3036. (in Chinese with English abstract)
	[汤俊兵, 肖燕, 安树青 (2010) 根茎克隆植物生态学研究进展. 生态学报, 30, 3028-3036.]
77	Thompson FL, Eckert CG (2004) Trade-offs between sexual and clonal reproduction in an aquatic plant: experimental manipulations vs. phenotypic correlations. Journal of Evolutionary Biology, 17, 581-592.
78	Touchette BW, Moody JW, Byrne CM, Marcus SE (2013) Water integration in the clonal emergent hydrophyte, Justicia americana: benefits of acropetal water transfer from mother to daughter ramets. Hydrobiologia, 702, 83-94.
79	van der Valk AG, Volin JC, Wetzel PR (2015) Predicted changes in interannual water-level fluctuations due to climate change and its implications for the vegetation of the Florida Everglades. Environmental Management, 55, 799-806.
80	van Drunen WE, Dorken ME (2012) Trade-offs between clonal and sexual reproduction in Sagittaria latifolia (Alismataceae) scale up to affect the fitness of entire clones. New Phytologist, 196, 606-616.
81	van Kleunen M, Fischer M (2001) Adaptive evolution of plastic foraging responses in a clonal plant. Ecology, 82, 3309-3319.
82	van Kleunen M, Fischer M, Schmid B (2000) Clonal integration in Ranunculus reptans: by-product or adaptation? Journal of Evolutionary Biology, 13, 237-248.
83	van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytologist, 166, 49-60.
84	Villamagna AM, Murphy BR (2010) Ecological and socio-economic impacts of invasive water hyacinth (Eichhornia crassipes): a review. Freshwater Biology, 55, 282-298.
85	Visser EJW, Bögemann GM, van de Steeg HM, Pierik R, Blom CWPM (2000) Flooding tolerance of Carex species in relation to field distribution and aerenchyma formation. New Phytologist, 148, 93-103.
86	Wang P, Xu YS, Dong BC, Xue W, Yu FH (2014) Effects of clonal fragmentation on intraspecific competition of a stoloniferous floating plant. Plant Biology, 16, 1121-1126.
87	Wang N, Yu FH, Li PX, He WM, Liu J, Yu GL, Song YB, Dong M (2009) Clonal integration supports the expansion from terrestrial to aquatic environments of the amphibious stoloniferous herb Alternanthera philoxeroides. Plant Biology, 11, 483-489.
88	Wang Z, Li Y, During HJ, Li L (2011) Do clonal plants show greater division of labour morphologically and physiologically at higher patch contrasts? PLoS ONE, 6, e25401.
89	Weisner SE, Strand JA (1996) Rhizome architecture in Phragmites australis in relation to water depth: implications for within-plant oxygen transport distances. Folia Geobotanica, 31, 91-97.
90	Wells CL, Pigliucci M (2000) Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants. Perspectives in Plant Ecology, Evolution and Systematics, 3, 1-18.
91	Wetzel RG (1988) Water as an environment for plant life. In: Vegetation of Inland Waters (ed. Symoens JJ), pp. 1-30. Kluwer Academic Publishers, Dordrecht.
92	White S, Ganf GG (2002) A comparison of the morphology, gas space anatomy and potential for internal aeration in Phragmites australis under variable and static water regimes. Aquatic Botany, 73, 115-127.
93	Wilsey B (2002) Clonal plants in a spatially heterogeneous environment: effects of integration on Serengeti grassland response to defoliation and urine-hits from grazing mammals. Plant Ecology, 159, 15-22.
94	Wolfer SR, Straile D (2004) Spatio-temporal dynamics and plasticity of clonal architecture in Potamogeton perfoliatus. Aquatic Botany, 78, 307-318.
95	Wu ZH, Yu D, Tu MH, Wang Q, Xiong W (2007) Interference between two floating-leaved aquatic plants: Nymphoides peltata and Trapa bispinosa. Aquatic Botany, 86, 316-320.
96	Xiao KY, Yu D, Wang JW (2006) Habitat selection in spatially heterogeneous environments: a test of foraging behaviour in the clonal submerged macrophyte Vallisneria spiralis. Freshwater Biology, 51, 1552-1559.
97	Xiao KY, Yu D, Xu XW, Xiong W (2007) Benefits of clonal integration between interconnected ramets of Vallisneria spiralis in heterogeneous light environments. Aquatic Botany, 86, 76-82.
98	Yan X (2003) Study of Ecological Response of Aquatic Plants to Stress. PhD dissertation, Wuhan University, Wuhan. (in Chinese with English abstract)
	[严雪 (2003) 水生植物的逆境生态学研究. 博士学位论文, 武汉大学, 武汉.]
99	Yan X, Wang HW, Wang QF, Rudstam LG (2013) Risk spreading, habitat selection and division of biomass in a submerged clonal plant: responses to heterogeneous copper pollution. Environmental Pollution, 174, 114-120.
100	Yan X, Yu D, Wang HY, Wang JW (2006) Response of submerged plant (Vallisneria spinulosa) clones to lead stress in the heterogenous soil. Chemosphere, 63, 1459-1465.
101	Ye XH, Yu FH, Dong M (2006) A trade-off between guerrilla and phalanx growth forms in Leymus secalinus under different nutrient supplies. Annals of Botany, 98, 187-191.
102	You WH, Fan SF, Yu D, Xie D, Liu CH (2014a) An invasive clonal plant benefits from clonal integration more than a co-occurring native plant in nutrient-patchy and competitive environments. PLoS ONE, 9, e97246.
103	You WH, Yu D, Xie D, Han C, Liu C (2014b) The invasive plant Alternanthera philoxeroides benefits from clonal integration in response to defoliation. Flora, 209, 666-673.
104	You WH, Yu D, Xie D, Yu LF, Xiong W, Han CM (2014c) Responses of the invasive aquatic plant water hyacinth to altered nutrient levels under experimental warming in China. Aquatic Botany, 119, 51-56.
105	Yu FH, Wang N, He WM, Dong M (2010) Effects of clonal integration on species composition and biomass of sand dune communities. Journal of Arid Environments, 74, 632-637.
106	Yu FH, Wang N, Alpert P, He WM, Dong M (2009) Physiological integration in an introduced, invasive plant increases its spread into experimental communities and modifies their structure. American Journal of Botany, 96, 1983-1989.
107	Zhang DY (2000) Researches on Theoretical Ecology. Higher Education Press, Beijing. (in Chinese)
	[张大勇 (2000) 理论生态学研究. 高等教育出版社, 北京.]
108	Zhang YY, Zhang DY, Barrett S (2010) Genetic uniformity characterizes the invasive spread of water hyacinth. Molecular Ecology, 19, 1774-1786.
109	Zhao CF, Li HL, Luo FL (2013) Effects of light heterogeneity on growth of a submerged clonal macrophyte. Plant Species Biology, 28, 156-164.
110	Zhou J, Wang D (2012) Survival strategies of stem fragments in narrow endemic and widespread plants of the aquatic genus Myriophyllum. Acta Hydrobiologica Sinica, 36, 316-322. (in Chinese with English abstract)
	[周洁, 王东 (2012) 狐尾藻属狭域种和广域种断枝的生长与再生能力比较研究. 水生生物学报, 36, 316-322.]
111	Zhu GR, Cao T, Zhang M, Ni LY, Zhang XL (2014) Fertile sediment and ammonium enrichment decrease the growth and biomechanical strength of submersed macrophyte Myriophyllum spicatum in an experiment. Hydrobiologia, 727, 109-120.
112	Zhu ZL, Li DZ, Wang XP, Sheng LJ, Shi Q (2007) Water physiology integration and its ecological effect of clonal plants. Acta Botanica Boreali-Occidentalia Sinica, 26, 2602-2614. (in Chinese with English abstract)
	[朱志玲, 李德志, 王绪平, 盛丽娟, 石强 (2007) 克隆植物的水分生理整合及其生态效应. 西北植物学报, 26, 2602-2614.]

[1]	Yanhui Li, Tianyuan Lan, Yue Wang, Yang Yu, Changming Zhao, Lihua Li, Wenting Xu, Guozhen Shen. Driving factors of spatial turnover of plant species in Shennongjia [J]. Biodiv Sci, 2022, 30(4): 21377-.
[2]	Yuan Sun, Weigang Hu, Shuran Yao, Ying Sun, Jianming Deng. Geographic patterns and environmental determinants of angiosperm and terrestrial vertebrate species richness in the Yellow River basin [J]. Biodiv Sci, 2020, 28(12): 1523-1532.
[3]	Changyan Zhou, Bin Wang, Yun Deng, Junjie Wu, Min Cao, Luxiang Lin. Canopy structure is an important factor driving local-scale woody plant functional beta diversity [J]. Biodiv Sci, 2020, 28(12): 1546-1557.
[4]	Shuoran Liu, Daode Yang, Xianfu Li, Lu Tan, Jun Sun, Xiaoyang He, Wenshu Yang, Guopeng Ren, Davide Fornacca, Qinghua Cai, Wen Xiao. Diversity in benthic and environmental characteristics on alpine micro-waterbodies and stream ecosystems in northwest Yunnan [J]. Biodiv Sci, 2019, 27(12): 1298-1308.
[5]	Hao Tian,Wanjin Liao. Consequences of clonal growth on pollinator visitation in flowering plants [J]. Biodiv Sci, 2018, 26(5): 468-475.
[6]	Hongyan Hu, Huan Chen, Huanli Xu. Main pollinators and their foraging behaviors on a sand-fixing legume, Thermopsis lanceolata, in Mu Us Sandland [J]. Biodiv Sci, 2012, 20(3): 354-359.
[7]	Yan Zhu, Fan Bai, Haifeng Liu, Wenchao Li, Liang Li, Guangqi Li, Shunzhong Wang, Weiguo Sang. Population distribution patterns and interspecific spatial associations in warm temperate secondary forests, Beijing [J]. Biodiv Sci, 2011, 19(2): 252-259.
[8]	Zhao Liu, Wei Zhou, Rengong Zhang, Yichang Xie, Qingwen Huang, Yunyan Wen. Foraging sites selection of green peafowl (Pavo muticus imperator) in different seasons in Shiyangjiang Valley of upper Yuanjiang drainage, Yunnan [J]. Biodiv Sci, 2008, 16(6): 539-546.
[9]	Xin Jia, Xingzhong Yang, Xiaoyun Pan, Bo Li, Jiakuan Chen. Vegetative propagation characteristics of Alternanthera philoxeroides in response to disturbances [J]. Biodiv Sci, 2008, 16(3): 229-235.
[10]	Yanbing Gong, Shuangquan Huang. On methodology of foraging behavior of pollinating insects [J]. Biodiv Sci, 2007, 15(6): 576-583.
[11]	Wang Xiaofan, ChenJiakuan. A survey on tbe habitats of rare and endangered aquatic plants in Hunan Province [J]. Biodiv Sci, 1994, 02(4): 193-198.