雌雄异株物种一把伞南星雌雄株空间分布及性别二态性

doi:10.17520/biods.2024084

摘要/Abstract

摘要：

雌雄异株是有花植物雌雄性别功能在个体水平上由结合到分离的重要进化转变之一, 发生于被子植物的多个科属。雌雄异株物种的雌雄个体通常在分布、形态等方面存在差异。研究其雌雄个体的空间分布及性别二态性, 是理解雌雄异株物种繁殖策略及其适应与进化的重要前提。天南星属(Arisaema)是天南星科内已报道唯一存在雌雄异株且较为进化的类群, 一把伞南星(A. erubescens)是该属中不同性别个体存在差异的多年生草本植物。本文以湖南省八大公山国家级自然保护区内分布的一把伞南星为研究对象, 通过研究其雌雄个体的空间分布、花期物候、形态结构及访花者类群, 以期明确该物种雌雄植株的空间关联性以及花期物候、形态结构的性别二态性。结果表明: 一把伞南星群体内性比均呈极显著雄性偏倚, 雌雄个体在小尺度范围呈聚集分布, 但在较大尺度上呈随机分布; 雄性个体比雌性个体更早进入花期, 置换多元方差分析显示雌雄植株间形态特征存在显著差异, 其中假茎基径、佛焰苞管部直径、花序基径、花序柄直径等特征对性别二态性有重要贡献; 主要传粉者为白天活动的菌蚊科菌蚊属(Mycetophila)的蕈蚊, 其对雄株的访问频率极显著高于雌株。这些结果表明: 雌雄异株物种一把伞南星不同性别植株的空间关联与其传粉者蕈蚊的活动习性相匹配, 其开花物候、形态特征及传粉者访问等方面的性别二态性是对繁殖成功的保障。

关键词: 一把伞南星, 雌雄异株, 性别二态性, 性比, 空间分布, 有性繁殖特征, 蕈蚊传粉

Abstract

Aims: The transition to dioecy constitutes a pivotal milestone in the evolution of sexual functions in flowering plants, marking a shift from the integration of male and female reproductive organs within the same individual to their separation. This sexual system occurs across numerous angiosperm families and genera. Both female and male individuals of dioecious species display variations in distribution, morphology, and life history traits. Therefore, it is essential to examine the spatial distribution and sexual dimorphism of dioecious species in order to comprehend their reproductive strategies, adaptability, and evolutionary patterns. The genus Arisaema is the only reported taxon within the Araceae family known to possess a dioecious sexual system. In this study, we explored the differences between the dioecious members of Arisaema erubescens in the Badagongshan National Nature Reserve, Hunan Province, China, with a specific focus on the spatial distribution and sexual dimorphisms.
Methods: We surveyed the coordinate positions of male and female individuals across four plots, analyzed both the sex ratio and spatial distribution patterns of these individuals. Sexual dimorphism was assessed based on phenological and morphological traits of A. erubescens. Additionally, a quantitative comparison of the floral visitor assemblages between female and male individuals was conducted.
Results: From our observations, the A. erubescens population was significantly dominated by staminate flora. Male and female individuals were found to clusters on small scales and disperse randomly on a large scale. The male individuals flowered 4 days earlier than the females. The permutational multivariate analysis of variance identified significant disparities in morphological traits between male and female individuals, which are pivotal to sexual dimorphism. These traits include the pseudostem basal diameter, the diameter of spathe tube, the inflorescence basal diameter, and the peduncle diameter. The primary pollinators of A. erubescens were the diurnal fungus gnats of the Mycetophila species, with an extremely higher visitation frequency observed on male individuals compared to those on female individuals.
Conclusions: Our study suggests that the spatial association of different genders in A. erubescens corresponds to the pollinators’ activity habits. The sex dimorphism of A. erubescens in flowering phenology, morphological traits, and pollination activity collectively guaranteed the reproductive success of the species.

Key words: Arisaema erubescens, dioecy, sex dimorphism, sex ratio, spatial distribution, sexual reproduction traits, pollination by fungus gnats

舒为杰, 何花, 曾罗, 谷志容, 谭敦炎, 杨晓琛 (2024) 雌雄异株物种一把伞南星雌雄株空间分布及性别二态性. 生物多样性, 32, 24084. DOI: 10.17520/biods.2024084.

Weijie Shu, Hua He, Luo Zeng, Zhirong Gu, Dunyan Tan, Xiaochen Yang (2024) Spatial distribution and sexual dimorphism of dioecious Arisaema erubescens. Biodiversity Science, 32, 24084. DOI: 10.17520/biods.2024084.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2024084

https://www.biodiversity-science.net/CN/Y2024/V32/I6/24084

图/表 8

图1 一把伞南星植株及花部形态示意图。(A)植株; (B)佛焰苞外部形态; (C)雌株佛焰苞纵切面观; (D)雄株佛焰苞纵切面观。1: 花序高度; 2: 假茎长; 3: 假茎基径; 4: 花序柄长; 5: 花序柄直径; 6: 佛焰苞长; 7: 佛焰苞檐宽; 8: 佛焰苞管长; 9: 管部直径; 10: 喉部直径; 11: 花序长; 12: 花序基径; 13: 花序顶径; 14: 附属器长; 15: 附属器直径; 16: 雄株佛焰苞基部小孔; 17: 通道直径。

Fig. 1 Schematic of individual and floral morphology of Arisaema erubescens. (A) Individual; (B) External morphology of spathe; (C) Female spathe vertical-section; (D) Male spathe vertical-section. 1, Inflorescence height; 2, Pseudostem length; 3, Pseudostem basal diameter; 4, Peduncle length; 5, Peduncle diameter; 6, Spathe length; 7, Limb width of spathe; 8, Tube length of spathe; 9, Tube diameter; 10, Throat diameter; 11, Inflorescence length; 12, Inflorescence basal diameter; 13, Inflorescence apical diameter; 14, Appendix length; 15, Appendix diameter; 16, Exit hole at the base of spathe in male individual; 17, Channel diameter.

表1 2022年八大公山国家级自然保护区一把伞南星在4个样方中的性比。P < 0.01表示性比极显著偏离1 : 1。

Table 1 Sex ratio of Arisaema erubescens in four samples in the Badagongshan National Nature Reserve in 2022. P < 0.01 indicates an extremely significant deviation from a 1 : 1 sex ratio.

样方 Sample	雄株 Male	雌株 Female	性比(雄 : 雌) Sex ratio (Male : Female)	G-检验 G-test	P
1	38	15	2.53	10.321	0.001
2	34	11	3.09	12.330	< 0.001
3	41	12	3.42	16.773	< 0.001
4	36	12	3.00	12.558	< 0.001

图2 2022年八大公山国家级自然保护区一把伞南星在4个样方中的空间分布

Fig. 2 Spatial distribution of Arisaema erubescens in four samples in the Badagongshan National Nature Reserve in 2022

图3 八大公山国家级自然保护区4个样方中一把伞南星雌雄植株间的空间关联。深色线为g(r)值, 浅色线为99%置信区间。

Fig. 3 Spatial associations between male and female individuals of Arisaema erubescens in four samples in the Badagongshan National Nature Reserve. The dark lines and light lines are g(r) values and 99% confidence envelopes, respectively.

图4 2022年(A)与2023年(B)八大公山国家级自然保护区一把伞南星种群花期动态

Fig. 4 Flowering phenology of Arisaema erubescens in the Badagongshan National Nature Reserve in 2022 (A) and 2023 (B)

表2 一把伞南星雌雄特征的比较(广义线性模型) (平均值 ± 标准误)。粗体表示具显著性差异(P < 0.05)特征中的较大值。

Table 2 Comparisons of traits between male and female individuals of Arisaema erubescens (generalized linear model, GLM) (mean ± SE). The larger value of significant differences (P < 0.05) is indicated in bold.

特征 Traits	雌株 Female individual	雄株 Male individual	Wald χ²	P
叶数 Leaf number	1.29 ± 0.08	1.00 ± 0.00	14.543	< 0.001
花序高度 Inflorescence height (cm)	57.40 ± 1.42	44.26 ± 1.35	44.899	< 0.001
假茎长 Pseudostem length (cm)	39.78 ± 2.05	26.65 ± 1.18	30.352	< 0.001
假茎基径 Pseudostem basal diameter (mm)	12.39 ± 0.44	7.85 ± 0.43	54.421	< 0.001
花序柄长 Peduncle length (cm)	9.76 ± 0.73	11.51 ± 0.57	3.530	0.06
花序柄直径 Peduncle diameter (mm)	4.91 ± 0.21	3.14 ± 0.15	48.564	< 0.001
佛焰苞长 Spathe length (mm)	76.26 ± 1.60	65.69 ± 2.60	12.219	< 0.001
佛焰苞檐宽 Limb width of spathe (mm)	45.96 ± 1.28	39.24 ± 1.19	1.044	0.307
佛焰苞管长Tube length of spathe (mm)	48.04 ± 1.69	42.14 ± 1.72	5.969	0.015
管部直径 Tube diameter (mm)	12.92 ± 0.26	8.89 ± 0.28	112.205	< 0.001
喉部直径 Throat diameter (mm)	15.46 ± 0.67	12.31 ± 0.50	14.079	< 0.001
花序长 Inflorescence length (mm)	21.71 ± 0.60	25.79 ± 0.85	15.551	< 0.001
花序基径 Inflorescence basal diameter (mm)	10.07 ± 0.29	5.35 ± 0.21	175.015	< 0.001
花序顶径 Inflorescence apical diameter (mm)	6.02 ± 0.15	3.70 ± 0.13	135.609	< 0.001
小花数 Number of floret	515.79 ± 22.48	263.04 ± 12.24	95.747	< 0.001
附属器长 Appendix length (mm)	38.76 ± 1.92	27.20 ± 1.62	21.014	< 0.001
附属器直径 Appendix diameter (mm)	4.95 ± 0.26	4.71 ± 0.26	0.430	0.512
小花直径 Floret diameter (mm)	1.17 ± 0.02	1.34 ± 0.03	32.098	< 0.001
出口孔截面积 Exit hole cross-sectional area (mm)	-	4.26 ± 0.36	-	-
通道直径 Channel diameter (mm)	-	2.00 ± 0.09	-	-

表2 一把伞南星雌雄特征的比较(广义线性模型) (平均值 ± 标准误)。粗体表示具显著性差异(P < 0.05)特征中的较大值。

特征 Traits	雌株 Female individual	雄株 Male individual	Wald χ²	P
叶数 Leaf number	1.29 ± 0.08	1.00 ± 0.00	14.543	< 0.001
花序高度 Inflorescence height (cm)	57.40 ± 1.42	44.26 ± 1.35	44.899	< 0.001
假茎长 Pseudostem length (cm)	39.78 ± 2.05	26.65 ± 1.18	30.352	< 0.001
假茎基径 Pseudostem basal diameter (mm)	12.39 ± 0.44	7.85 ± 0.43	54.421	< 0.001
花序柄长 Peduncle length (cm)	9.76 ± 0.73	11.51 ± 0.57	3.530	0.06
花序柄直径 Peduncle diameter (mm)	4.91 ± 0.21	3.14 ± 0.15	48.564	< 0.001
佛焰苞长 Spathe length (mm)	76.26 ± 1.60	65.69 ± 2.60	12.219	< 0.001
佛焰苞檐宽 Limb width of spathe (mm)	45.96 ± 1.28	39.24 ± 1.19	1.044	0.307
佛焰苞管长Tube length of spathe (mm)	48.04 ± 1.69	42.14 ± 1.72	5.969	0.015
管部直径 Tube diameter (mm)	12.92 ± 0.26	8.89 ± 0.28	112.205	< 0.001
喉部直径 Throat diameter (mm)	15.46 ± 0.67	12.31 ± 0.50	14.079	< 0.001
花序长 Inflorescence length (mm)	21.71 ± 0.60	25.79 ± 0.85	15.551	< 0.001
花序基径 Inflorescence basal diameter (mm)	10.07 ± 0.29	5.35 ± 0.21	175.015	< 0.001
花序顶径 Inflorescence apical diameter (mm)	6.02 ± 0.15	3.70 ± 0.13	135.609	< 0.001
小花数 Number of floret	515.79 ± 22.48	263.04 ± 12.24	95.747	< 0.001
附属器长 Appendix length (mm)	38.76 ± 1.92	27.20 ± 1.62	21.014	< 0.001
附属器直径 Appendix diameter (mm)	4.95 ± 0.26	4.71 ± 0.26	0.430	0.512
小花直径 Floret diameter (mm)	1.17 ± 0.02	1.34 ± 0.03	32.098	< 0.001
出口孔截面积 Exit hole cross-sectional area (mm)	-	4.26 ± 0.36	-	-
通道直径 Channel diameter (mm)	-	2.00 ± 0.09	-	-

图5 八大公山国家级自然保护区一把伞南星两种性别表型植株特征的主成分分析

Fig. 5 Principal component (PC) analysis of traits in two sex phenotypes of Arisaema erubescens in the Badagongshan National Nature Reserve

图6 不同访花者对一把伞南星雌雄花序的访花频率(A)及访花者数量日动态(B) (平均值 ± 标准误)。**表示雌雄个体间传粉者访花频率在P < 0.01水平下存在极显著差异; ns表示雌雄个体间传粉者访花频率不存在显著差异(P ≥ 0.05); (B)图中不同大、小写字母分别表示雄、雌花序在一天内不同时段的访花次数在P < 0.05水平下差异显著。

Fig. 6 Visit frequency by different visitors between male and female inflorescences (A) and temporal dynamics of the visitors number (B) of Arisaema erubescens (mean ± SE). ** indicates significant difference of visit frequency between male and female individuals at P < 0.01, while ns indicates no significant difference. Different capital and lowercase letters in (B) indicate significantly different visitor number in male and female inflorescences between different time of the day at P < 0.05, respectively.

参考文献 59

[1]	Abe T (2001) Flowering phenology, display size, and fruit set in an understory dioecious shrub, Aucuba japonica (Cornaceae). American Journal of Botany, 88, 455-461. PMID
[2]	Andreadis SS, Cloonan KR, Myrick AJ, Chen HB, Baker TC (2015) Isolation of a female-emitted sex pheromone component of the fungus gnat, Lycoriella ingenua, attractive to males. Journal of Chemical Ecology, 41, 1127-1136. DOI PMID
[3]	Ashman TL (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology, 81, 2577-2591.
[4]	Avila Jr RS, Freitas L (2011) Frequency of visits and efficiency of pollination by diurnal and nocturnal lepidopterans for the dioecious tree Randia itatiaiae (Rubiaceae). Australian Journal of Botany, 59, 176-184.
[5]	Baddeley AJ, Rubak E, Turner R (2015) Spatial Point Ptterns:Methodology and Applications with R. Chapman and Hall, New York.
[6]	Barrett SCH (1992) Gender variation and the evolution of dioecy in Wurmbea dioica (Liliaceae). Journal of Evolutionary Biology, 5, 423-444.
[7]	Barrett SCH (2008) Major evolutionary transitions in flowering plant reproduction: An overview. International Journal of Plant Sciences, 169, 1-5.
[8]	Barrett SCH, Hough J (2013) Sexual dimorphism in flowering plants. Journal of Experimental Botany, 64, 67-82. DOI PMID
[9]	Barrett SCH, Yakimowski SB, Field DL, Pickup M (2010) Ecological genetics of sex ratios in plant populations. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 2549-2557.
[10]	Barriault I, Barabé D, Cloutier L, Gibernau M (2010) Pollination ecology and reproductive success in Jack-in-the-pulpit (Arisaema triphyllum) in Quebéc (Canada). Plant Biology, 12, 161-171. DOI PMID
[11]	Bedhomme S, Chippindale AK (2007) Irreconcilable differences: When sexual dimorphism fails to resolve sexual conflict. In: Sex, Size and Gender Roles (eds Fairbairn DJ, Blanckenhorn WU, Szekely T),pp. 185-194. Oxford University Press, Oxford.
[12]	Bullock SH, Bawa KS (1981) Sexual dimorphism and the annual flowering pattern in Jacaratia dolichaula (D-Smith) Woodson (Caricaceae) in a Costa Rican rain forest. Ecology, 62, 1494-1504.
[13]	Charlesworth D (1999) Theories on the evolution of dioecy. In: Gender and Sexual Dimorphism in Flowering Plants (eds Geber MA, Dawson TE, Delph LF). pp. 33-60. Springer, Berlin.
[14]	Dawson TE, Geber MA (1999) Dimorphism in physiology and morphology. In: Gender and Sexual Dimorphism in Flowering Plants (eds Geber MA, Dawson TE, Delph LF),pp.176-215. Springer, Berlin.
[15]	Delph LF, Ashman TL (2006) Trait selection in flowering plants: How does sexual selection contribute? Integrative and Comparative Biology, 46, 465-472. DOI PMID
[16]	Delph LF, Galloway LF, Stanton ML (1996) Sexual dimorphism in flower size. The American Naturalist, 148, 299-320.
[17]	Doust JL, Cavers P (1982) Sex and gender dynamics in Jack-in-the-pulpit, Arisaema triphyllum (Araceae). Ecology, 63, 797-808.
[18]	Dudley LS (2006) Ecological correlates of secondary sexual dimorphism in Salix glauca (Salicaceae). American Journal of Botany, 93, 1775-1783. DOI PMID
[19]	Hu DM, Yao RX, Chen Y, You XS, Wang SY, Tang XX, Wang XY (2021) Tirpizia sinensis improves pollination accuracy by promoting the compatible pollen growth. Biodiversity Science, 29, 887-896. (in Chinese with English abstract)
	[胡德美, 姚仁秀, 陈燕, 游贤松, 王顺雨, 汤晓辛, 王晓月 (2021) 青篱柴通过促进亲和花粉生长而提高传粉精确性. 生物多样性, 29, 887-896.]
[20]	Hu GW (2008) Reproductive Studies on Arisaema yunnanense Buchet and A. erubescens (Wall.) Schott. PhD dissertation, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming. (in Chinese with English abstract)
	[胡光万 (2008) 山珠南星和一把伞南星的繁殖生物学研究. 博士学位论文, 中国科学院昆明植物研究所, 昆明.]
[21]	Jiménez PD, Hentrich H, Aguilar-Rodríguez PA, Krömer T, Chartier M, Gibernau M (2019) A review on the pollination of aroids with bisexual flowers. Annals of the Missouri Botanical Garden, 104, 83-104. DOI
[22]	Kakishima S, Tuno N, Hosaka K, Okamoto T, Ito T, Okuyama Y (2019) A specialized deceptive pollination system based on elaborate mushroom mimicry. bioRxiv, doi: 10.1101/819136.
[23]	Kinoshita E (1986) Size-sex relationship and sexual dimorphism in Japanese Arisaema (Araeeae). Ecological Research, 1, 157-171.
[24]	Kostelc JG, Girard JE, Hendry LB (1980) Isolation and identification of a sex attractant of a mushroom-infesting sciarid fly. Journal of Chemical Ecology, 6, 1-11.
[25]	Li H (1980) Himalayas-Hengduan Mountains——The centre of distribution and differentiation of the genus Arisaema——To discuss the problems about the origin and migration of this genus. Acta Botanica Yunnanica, 2, 402-416. (in Chinese with English abstract)
	[李恒 (1980) 喜马拉雅-横断山脉是天南星属的分布中心和分化中心——兼论天南星属的起源和扩散. 云南植物研究, 2, 402-416.]
[26]	Liu DX, Wang QF, Yang CF (2022) Flower diversity and pollination strategy in Araceae. Biodiversity Science, 30, 21426. (in Chinese with English abstract) DOI
	[刘德鑫, 王青锋, 杨春锋 (2022) 天南星科植物的花多样性与传粉策略. 生物多样性, 30, 21426.] DOI
[27]	Lloyd DG, Webb CJ (1977) Secondary sex characters in plants. Botanical Reviews, 43, 177-216.
[28]	Lu ZJ, Liu FL, Wu H, Jiang MX (2015) Species composition, size class, and spatial patterns of snags in the Badagongshan (BDGS) mixed evergreen and deciduous broad-leaved forest in Central China. Biodiversity Science, 23, 167-173. (in Chinese with English abstract) DOI
	[卢志军, 刘福玲, 吴浩, 江明喜 (2015) 八大公山常绿落叶阔叶混交林枯立木物种组成、大小级与分布格局. 生物多样性, 23, 167-173.] DOI
[29]	Matsuhisa S, Ushimaru A (2015) Sexual dimorphism in floral longevity and flowering synchrony in relation to pollination and mating success in three dioecious Ilex species. American Journal of Botany, 102, 1187-1197. DOI PMID
[30]	Matsumoto TK, Hirobe M, Akaji Y, Miyazaki Y (2020) Population structures and spatial patterns of two unpalatable Arisaema species (Araceae) with and without clonal reproduction in a riparian forest intensively grazed by Sika deer. Journal of Forestry Research, 31, 155-162.
[31]	Matsumoto TK, Hirobe M, Sueyoshi M, Miyazaki Y (2021) Selective pollination by fungus gnats potentially functions as an alternative reproductive isolation among five Arisaema species. Annals of Botany, 127, 633-644. DOI PMID
[32]	Matsumoto TK, Miyazaki Y, Sueyoshi M, Senda Y, Yamada K, Hirobe M (2019) Pre-pollination barriers between two sympatric Arisaema species in northern Shikoku Island, Japan. American Journal of Botany, 106, 1612-1621. DOI PMID
[33]	Mcalpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (1981) Manual of Nearctic Diptera, Vol. 1. Research Branch Agriculture Canada, Ottawa.
[34]	Mercer CA, Eppley SM (2010) Inter-sexual competition in a dioecious grass. Oecologia, 164, 657-664. DOI PMID
[35]	Midgley JJ (2010) Causes of secondary sexual differences in plants—Evidence from extreme leaf dimorphism in Leucadendron (Proteaceae). South African Journal of Botany, 76, 588-592.
[36]	Moquet L, Lateur L, Jacquemart AL, De Cauwer I, Dufay M (2020) Temporal dynamics of sexual dimorphism in a dioecious species. Annals of Botany, 126, 471-480. DOI PMID
[37]	Obeso JR (2002) The costs of reproduction in plants. New Phytologist, 155, 321-348. DOI PMID
[38]	Ohi-Toma T, Wu S, Murata H, Murata J (2016) An updated genus-wide phylogenetic analysis of Arisaema (Araceae) with reference to sections. Botanical Journal of the Linnean Society, 182, 100-114.
[39]	Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Solymos P, Stevens MHH, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, Caceres MD, Durand S, Evangelista HBA, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill MO, Lahti L, McGlinn D, Ouellette MH, Cunha ER, Smith T, Stier A, Braak CJFT, Weedon J (2022) Vegan: Community Ecology Package. R Package Version 2.6-4. https://cran.r-project.org/web/packages/vegan/index.html/. (accessed on 2022-04-20)
[40]	Pickup M, Barrett SCH (2012) Reversal of height dimorphism promotes pollen and seed dispersal in a wind-pollinated dioecious plant. Biology Letters, 8, 245-248. DOI PMID
[41]	Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany, 101, 1588-1596. DOI PMID
[42]	Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. American Journal of Botany, 82, 596-606.
[43]	Richardson CR, Clay K (2001) Sex-ratio variation among Arisaema species with different patterns of gender diphasy. Plant Species Biology, 16, 139-149.
[44]	Rodriguez-Riano T, Dafni A (2000) A new procedure to asses pollen viability. Sexual Plant Reproduction, 12, 241-244.
[45]	Sinclair JP, Emlen J, Freeman DC (2012) Biased sex ratios in plants: Theory and trends. Botanical Reviews, 78, 63-86.
[46]	Song B, Chen G, Stöcklin J, Peng DL, Niu Y, Li ZM, Sun H (2014) A new pollinating seed-consuming mutualism between Rheum nobile and a fly fungus gnat, Bradysia sp., involving pollinator attraction by a specific floral compound. New Phytologist, 203, 1109-1118. DOI PMID
[47]	Steven JC, Delph LF, Brodie ED III (2007) Sexual dimorphism in the quantitative-genetic architecture of floral, leaf, and allocation traits in Silene latifolia. Evolution, 61, 42-57. PMID
[48]	Suetsugu K, Nishigaki H, Fukushima S, Ishitani E, Kakishima S, Sueyoshi M (2022) Thread-like appendix on Arisaema urashima (Araceae) attracts fungus gnat pollinators. Ecology, 103, e3782.
[49]	Suetsugu K, Sato R, Kakishima S, Okuyama Y, Sueyoshi M (2021) The sterile appendix of two sympatric Arisaema species lures each specific pollinator into deadly trap flowers. Ecology, 102, e03242.
[50]	Ushimaru A, Seo N, Sakagami K, Funamoto D (2023) Sexual dimorphism in a dioecious species with complex, specialist- pollinated flowers. American Journal of Botany, 110, e16148.
[51]	Vamosi JC, Otto SP, Barrett SCH (2003) Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. Journal of Evolutionary Biology, 16, 1006-1018. PMID
[52]	Vitale JJ, Freeman DC (1986) Partial niche separation in Spinacia oleracea L.: An examination of reproductive allocation. Evolution, 40, 426-430.
[53]	Vogel S, Martens J (2000) A survey of the function of the lethal kettle traps of Arisaema (Araceae), with records of pollinating fungus gnats from Nepal. Botanical Journal of the Linnean Society, 133, 61-100.
[54]	Wu ZY, Li H (1979) Flora Reipublicae Popularis Sinicae, Tomus 13(2). Science Press, Beijing. (in Chinese)
	[吴征镒, 李恒 (1979) 中国植物志(第十三卷第二分册). 科学出版社, 北京.]
[55]	Yi TS, Li H, Li DZ (2002) The course of change and development of the classification systems of the Araceae. Journal of Wuhan Botanical Research, 20, 48-61. (in Chinese with English abstract)
	[伊廷双, 李恒, 李德铢 (2002) 天南星科分类系统的沿革. 武汉植物学研究, 20, 48-61.]
[56]	Yu Q, Barrett SCH, Wang XJ, Zhong L, Wang H, Li DZ, Zhou W (2022) Sexual dimorphism, temporal niche differentiation, and evidence for the Jack Sprat effect in an annual dioecious plant. Journal of Systematics and Evolution, 60, 1078-1091. DOI
[57]	Zeng L, Shu WJ, He H, Li T, Yang XC, Li L (2023) Post-pollination barriers contribute to coexistence of partially pollinator-sharing Arisaema species (Araceae). Ecology and Evolution, 13, e10696.
[58]	Zeng ZH, Yu Q, Feng QH, Wang XJ, Zhong L, Sun HY, Wang H, Li DZ, Barrett SCH, Zhou W (2023) Functional consequences of temporal reversal of height dimorphism for pollen and seed dispersal in a dioecious plant. Journal of Systematics and Evolution, 62, 438-448.
[59]	Zhang DY (2004) Plant Life-History Evolution and Reproductive Ecology. Science Press, Beijing. (in Chinese)
	[张大勇 (2004) 植物生活史进化与繁殖生态学. 科学出版社, 北京.]