小果野芭蕉种子散布和不同时空尺度上种子被捕食格局

doi:10.3773/j.issn.1005-264x.2008.01.015

摘要/Abstract

摘要：

以分布在云南西双版纳地区的大型先锋草本植物小果野芭蕉(Musa acuminata)为研究材料,研究其种子初次散布过程和不同时空尺度上种子被捕食格局。小果野芭蕉的成熟果实有75%在夜间被取食和传播,在白天消失的果实则占25%。蝙蝠是其最主要的种子传播者,鸟类在其种子传播过程中也起到一定的作用。人工摆放种子试验结果显示小果野芭蕉种子的主要转移者是小型啮齿类(鼠类)和蚁类:在开放处理下3 d后转移率为86%,排除蚁类(鼠类可进入)处理下种子转移率为69%以及排除鼠类(蚂蚁可进入)处理下种子被转移率为56%。季节、地点和生境均显著影响人工摆放种子被转移强度:雨季显著高于旱季(p<0.001),野芭蕉生境显著高于与其相连的自然森林和荒地(p<0.001),在人为干扰较少的补蚌自然保护区显著低于西双版纳热带植物园和新山,而后两者之间并无显著差异(p>0.05)。同时,地点和生境以及季节、地点和生境都有显著的交互作用。与相邻的森林和荒地相比,野芭蕉群落中种子被鼠类捕食的强度最大且受蚁类二次转移的比例最少,森林和荒地中种子被鼠类捕食的强度相对较小且蚁类对种子的二次转移比例较高,从而更好地帮助种子逃避鼠类捕食。因此,依赖于食果动物(主要是蝙蝠, 也包括鸟类)的初次散布是小果野芭蕉种子逃避捕食的关键。

关键词: 小果野芭蕉, 种子散布, 种子转移, 时空差异, 蝙蝠, 鼠类, 蚁类, 西双版纳

Abstract:

Aims Seed dispersal and seed predation are important on mechanisms of forest maintenance and degeneration. Understanding them can enable effective conservation measures, especially in Xishuangbanna tropical rainforest in China which is suffering severe pressures.
Methods Musa acuminata is a large herbaceous plant in Xishuangbanna, Yunnan Province. We investigated seed dispersal and spatial-temporal variation of seed predation in three habitats (wild banana communities, virgin rainforest and open habitat) in three different sites of Xishuangbanna (XTBG, Xinshan and Bubeng). We used two treatments excluding ants and rodents and surveyed community structure of ants and rodents to explore the relationship between abundance of predators and intensity of seed predation.
Important findings Bats were the most important, effective seed disperser, and birds also played an important role in seed dispersal, with approximately 75% of the mature fruits of M. acuminata dispersed at night and about 25% during daytime. After primary dispersal, seeds of M. acuminata were mainly removed by small rodents and ants. This seed predation was significantly influenced by season, site and habitat. Seed predation was significantly stronger in rainy than dry seasons (p<0.001). Seed predation in M. acuminata communities was the highest among the three habitats (p<0.001), and seed predation in Bubeng Nature Reserve, which had the least disturbance, was significantly lower than the other two sites (which were not significantly different at p>0.05). Seed removal was generally consistent with the abundance of rodents and ants in different seasons, habitats and sites. The interaction between sites and habitats and the interaction among seasons, sites and habitats had significant effects on seed predation. Compared to nearby forest and open habitats, Musa communities had the most abundant rodents and the highest seed predation and the lowest proportion of secondary seed dispersal by ants. In contrast, seed predation by rodents in forest and open habitat was relatively weak and a large proportion of post dispersal seed was removed by ants. Therefore, primary seed dispersal mostly by bats and birds is essential for M. acuminata seeds to escape seed predation.

Key words: Musa acuminata, spatial-temporal variation, seed dispersal, seed removal, Xishuangbanna

孟令曾, 高秀霞, 陈进. 小果野芭蕉种子散布和不同时空尺度上种子被捕食格局. 植物生态学报, 2008, 32(1): 133-142. DOI: 10.3773/j.issn.1005-264x.2008.01.015

MENG Ling-Zeng, GAO Xiu-Xia, CHEN Jin. SEED DISPERSAL AND SPATIAL-TEMPORAL VARIATION OF SEED PREDATION OF MUSA ACUMINATA IN XISHUANGBANNA, SOUTHWEST CHINA. Chinese Journal of Plant Ecology, 2008, 32(1): 133-142. DOI: 10.3773/j.issn.1005-264x.2008.01.015

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.plant-ecology.com/CN/10.3773/j.issn.1005-264x.2008.01.015

https://www.plant-ecology.com/CN/Y2008/V32/I1/133

图/表 12

表1 研究地点和概况

Table 1 Study sites and the general information

	地点1 Site1	地点2 Site2	地点3 Site3
位置 Location	XTBG	XS	BB
经纬度 Latitude & longitude	21°56' N, 101°15' E	21°50' N, 101°33' E	21°37' N, 101°35' E
海拔 Altitude (m)	570	960	680
野芭蕉群落面积 Area of Musa communities (hm²)	2~3	3~4	4~5

图1 小果野芭蕉种子散布观察试验 a: 对照 Control b: 排除攀缘动物 Climbing animal excluded c: 排除飞行动物 Aviate animal excluded

Fig.1 Illustration of the observation for seed dispersal of Musa acuminata

图2 不同处理下果实在白天和夜晚的丢失比例数据点为平均值±标准误 Data are means±SE (N=8) 不同小写字母表示差异显著(p<0.001) Bars with different letters are significantly different (p<0.001) 1. 对照 Control 2. 排除攀缘动物 Climbing animal excluded 3. 排除飞行动物 Aviate animal excluded

Fig.2 Proportion of fruit removed under different treatment during day and night respectively

图3 不同处理下种子剩余率数据点为平均值±标准误 Data are means±SE (N=630) 不同小写字母表示差异显著(p<0.05) Bars with different letters are significantly different (p<0.05) 1.开放对照 Open CK 2.蚁类排除 Ants excluded 3.鼠类排除 Rats excluded

Fig.3 Percentage of seed remained under different treatment (indicated by the percentage of seed remained)

图4 开放处理下不同季节(图a:N旱季=360,N雨季=270)、不同地点(图b:N=210)、不同生境(图c:N=210)以及地点和生境的交互作用(图d:N=70)对小果野芭蕉种子二次散布的影响(用剩余种子百分数表示) 数据点为平均值±标准误, 不同小写字母表示差异显著(p<0.05) S代表地点,1、2和3依次为西双版纳热带植物园(XTBG)、新山(XS)和补蚌(BB);M代表生境,1、2和3分别为野芭蕉群落(WB)、森林(FR)和荒地(OH)

Fig.4 The effect of different season (Fig. a: Ndry season=360, Nrainy season=270), different site(Fig. b: N=210), different habitat (Fig. c: N=210) and the interaction between site and habitat (Fig. d: N=70) on the secondary seed dispersal of Musa acuminata under open treatment (indicated by percentage of seed remained) Data are means±SE, bars with different letters are significantly different (p<0.05) S represents different site, 1, 2 and 3 means Xishuangbanna Tropical Botanical Garden, Xinshan and Bubeng respectively; M represents different habitat, 1, 2 and 3 means Musa community (WB), Forest (FR) and Open habitat (OH)

表3 排除蚁类处理下季节、地点和生境对种子二次散布影响的多因素方差分析

Table 3 MVA of the effects of season, site and habitat on the secondary seed dispersal of Musa acuminata under ants excluded treatment

	df	MS	F	p
季节 Season	1	35.493	3.112	0.078^ns
地点 Site	2	180.322	15.809	0.000^***
生境 Habitat	2	188.358	16.513	0.000^***
季节×地点 Season×site	2	170.986	14.990	0.000^***
季节×生境 Season×habitat	2	47.431	4.158	0.016^*
地点×生境 Site×habitat	4	196.191	17.200	0.000^***
季节×地点×生境 Season×site×habitat	4	115.888	10.160	0.000^***
误差 Error	612	11.407
合计 Total	630

图5 蚁类排除处理下,不同地点(图a: N=210)和不同生境(图b: N=210对小果野芭蕉种子二次散布的影响(用剩余种子百分数表示) 数据点为平均值±标准误,不同小写字母表示差异显著(p<0.05) XTBG、XS、BB、WB、FR、OH: 见图4

Fig.5 The effect of different site (Fig. a:N=210) and different habitat (Fig. b: N=210) on the secondary seed dispersal of Musa acuminata under ants excluded treatment (indicated by percentage of seed remained) Data are means±SE, Bars with different letters are significantly different (p<0.05) XTBG、XS、BB、WB、FR、OH: See Fig. 4

图6 鼠类排除处理下,不同地点(图a: N=210)和不同生境(图b: N=210对小果野芭蕉种子二次散布的影响(用剩余种子百分数表示) 数据点为平均值±标准误,不同小写字母表示差异显著(p<0.05) XTBG、XS、BB、WB、FR、OH: 见图4

Fig.6 The effect of different site (Fig. a:N=210)and different habitat (Fig. b: N=210) on the secondary seed dispersal of Musa acuminata under rats excluded treatment (indicated by percentage of seed remained) Data are means±SE, Bars with different letters are significantly different (p<0.05) XTBG、XS、BB、WB、FR、OH: See Fig. 4

表4 排除鼠类处理下季节、地点和生境对种子二次散布的多因素方差分析

Table 4 MVA of the effects of season, site and habitat on the secondary seed dispersal of Musa acuminata under rats excluded treatment

	df	MS	F	p-value
季节 Season	1	29.484	2.506	0.039^*
地点 Site	2	115.053	9.660	0.000^***
生境 Habitat	2	167.416	14.057	0.000^***
季节×地点 Season×site	2	113.519	9.531	0.000^***
季节×生境 Season×habitat	2	43.911	3.687	0.026^*
地点×生境 Site×habitat	4	29.142	2.447	0.045^*
季节×地点×生境 Season×site×habitat	4	155.547	13.060	0.000^***
误差 Error	612	11.910
合计 Total	630

表2 开放处理下季节、地点和生境对种子二次散布影响的多因素方差分析

Table 2 MVA of the effects of season, site and habitat on the secondary seed dispersal of Musa acuminata under open treatment

	df	MS	F	p
季节 Season	1	274.667	31.286	0.000^***
地点 Site	2	47.114	5.366	0.005^**
生境 Habitat	2	111.905	12.746	0.000^***
季节×地点 Season×site	2	0.879	0.100	0.905^ns
季节×生境 Season×habitat	2	11.804	1.344	0.261^ns
地点×生境 Site×habitat	4	43.776	4.986	0.001^***
季节×地点×生境 Season×site×habitat	4	36.703	4.181	0.002^**
误差 Error	612	8.779
合计 Total	630

图7 蚁类排除和鼠类排除处理下,季节和地点的交互作用(图a: N旱季=360,N雨季=270)、季节和生境的交互作用(图b: N旱季=360,N雨季=270)以及地点和生境的交互作用(图c: N=70)对小果野芭蕉种子二次散布的影响(用剩余种子百分数表示) 数据点为平均值±标准误,不同小写字母表示差异显著(p<0.05)。D代表旱季;R代表雨季;S代表地点,1、2和3依次为西双版纳热带植物园(XTBG)、新山(XS)和补蚌(BB);M代表生境,1、2和3分别为野芭蕉群落(WB)、森林(FR)和荒地(OH)

Fig.7 The effect of season and site interaction (Fig. a: Ndry season=360,Nrainy season=270), season and habitat interaction (Fig. b: Ndry season=360,Nrainy season=270), site and habitat interaction (Fig. c: N=70) on the secondary seed dispersal of Musa acuminata under ants excluded and rats excluded treatment (indicated by percentage of seed remained) Data are means±SE, bars with different letters are significantly different (p<0.05). D and R represents dry and rainy season respectively; S represents different site, 1, 2 and 3 means Xishuangbanna Tropical Botanical Garden, Xinshan and Bubeng respectively; M represents different habitat, 1, 2 and 3 mean Musa community, forest and open habitat

表5 不同季节、地点和生境鼠类和蚁类的群落调查结果

Table 5 Species number and amount of rats and ants in different season, site and habitat

种类 Species		旱季 Dry season	雨季 Rain season	XTBG	XS	BB	野芭蕉群落 Musa community	森林 Forest	荒地 Open habitat	合计 Total
鼠类 Rats	物种数 Number of species	8	5	6	5	7	8	4	4	9
	个体总数 Total amounts	47	50	32	30	35	48	42	7	97
蚁类 Ants	物种数 Number of species	72	53	46	64	49	41	49	61	104
	个体总数 Total amounts	1 778	822	469	1 310	821	491	411	1 698	2 600

参考文献 37

[1]	Allmen CV, Morellato LPC, Pizo MA (2004). Seed predation under high seed density condition: the palm Euterpe edulis in the Brazilian Atlantic Forest. Journal of Tropical Ecology, 20, 471-474.
[2]	Baker HG (1974). The evolution of weeds. Annual Review of Ecology and Systematics, 5, 1-24.
[3]	Basu P (1997). Seasonal and spatial patterns in ground foraging ants in a rainforest in the western Ghats, India. Biotropica, 29, 489-500.
[4]	Benkman CW, Parchman TL, Favis A, Siepielski AM (2003). Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. The American Naturalist, 162, 182-194.
[5]	Brewer SW (2001). Predation and dispersal of large and small seeds of a tropical palm. Oikos, 92, 245-255.
[6]	Chen F (陈帆), Chen J (陈进), Liu ZQ (刘志秋), Zhang L (张玲), Liu Y (刘勇), Bai ZL (白智林) (2004). The role of ants in seed dispersal of Globba lancangensis and the spatial distribution of its seedlings. Acta Phytoecologica Sinica (植物生态学报), 28, 210-217. (in Chinese with English abstract)
[7]	Connell JH (1971). On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: den Boer BJ, Gradwell GR eds. Dynamics of Population. Centre for Agricultural Publishing and Documentation, Wageningen, 298-310.
[8]	Davidson DW, Morton SR (1981). Myrmecochory in some plants (F. Chenopodiaceae) of the Australian arid zone. Oecologia, 50, 357-366.
[9]	Díaz M (1992). Spatial and temporal patterns of granivorous ant seed predation in patchy cereal crop areas of central Spain. Oecologia, 91, 561-568.
[10]	Elangovan V, Marimuthu G, Kunz TH (1999). Temporal patterns of individual and group foraging behaviour in the short-nosed fruit bat, Cynopterus sphinx, in South India. Journal of Tropical Ecology, 15, 681-687.
[11]	Fedriani JM, Manzaneda AJ (2005). Pre- and postdispersal seed predation by rodents: balance of food and safety. Behavioral Ecology, 16, 1018-1024.
[12]	Forget PM, Milleron T (1991). Evidence for secondary seed dispersal by rodents in Panama. Oecologia, 87, 596-599.
[13]	García-Casta†o JL, Kollmann J, Jordano P (2006). Spatial variation of post-dispersal seed removal by rodents in highland microhabitats of Spain and Switzerland. Seed Science Research, 16, 213-222.
[14]	Howe HF, Smallwood J (1982). Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201-228.
[15]	Hulme PE (1993). Post-dispersal seed predation by small mammals. Symposium of the Zoological Society of London, 65, 269-287.
[16]	Hulme PE (1994). Post-dispersal seed predation in grassland: its magnitude and sources of variation. Journal of Ecology, 82, 645-652.
[17]	Hulme PE, Kollmann J (2005). Seed predator guilds, spatial variation in post-dispersal seed predation and potential effects on plant demography- a temperate perspective. In: Forget PM, Lambert JE, Hulme PE, van der Wall SB eds. Seed Fate: Predation, Dispersal and Seedling Establishment. CABI Publishing, Wallingford, 9-30.
[18]	Janzen DH (1970). Herbivores and the number of tree species in tropical forests. American Naturalist, 104, 501-528.
[19]	Janzen DH (1971). Seed predation by animals. Annual Review of Ecology and Systematics, 2, 465-492.
[20]	Leal IR, Oliveira PS (1998). Interactions between fungus-growing ants (Attini), fruits and seeds in Cerrado vegetation in Southeast Brazil. Biotropica, 30, 170-178.
[21]	Levey DJ, Byrne MM (1993). Complex ant-plant interactions: rain-forest ants as secondary dispersers and post-dispersal seed predators. Ecology, 74, 1802-1812.
[22]	Liu AZ (刘爱忠) (2001). Phylogeny and Biogeography of Musaceae (芭蕉科植物的系统演化与生物地理学). PhD dissertation, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming. (in Chinese with English abstract)
[23]	Manson RH, Stiles EW (1998). Links between microhabitat preferences and seed predation by small mammals in old fields. Oikos, 82, 37-50.
[24]	Medellín RA, Gaona O (1999). Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, México. Biotropica, 31, 478-485.
[25]	Myster RW (2003). Effects of species, density, patch-type, and season on post-dispersal seed predation in a Puerto-Rican pasture. Biotropica, 35, 542-546.
[26]	Robinson JV, Dickerson JE Jr (1987). Does invasion sequence affect community structure? Ecology, 68, 587-595.
[27]	Schupp EW, Fuentes M (1995). Spatial patterns of seed dispersal and the unification of plant population ecology. Ecoscience, 2, 267-275.
[28]	Shepherd VE, Chapman CA (1998). Dung beetles as secondary seed dispersers: impact on seed predation and germination. Journal of Tropical Ecology, 14, 199-215.
[29]	Shugart HH (1998). Terrestrial Ecosystems in Changing Environments. Cambridge University Press, Cambridge, 103-143.
[30]	Simmonds NW (1962). The Evolution of the Bananas. Longmans, Green & Co. Ltd., London.
[31]	Tang ZH (唐占辉), Cao M (曹敏), Sheng LX (盛连喜), Liang B (梁冰), Zhang SY (张树义) (2005). Fruit consumption and seed dispersal of wild banana Musa acuminata by short-nosed fruit bat Cynopterus sphinx. Acta Zoologica Sinica (动物学报), 51, 608-615. (in Chinese with English abstract)
[32]	Thomas DW, Cloutier D, Provencher M, Houle C (1988). The shape of bird- and bat-generated seed shadows around a tropical fruiting tree. Biotropica, 20, 347-348.
[33]	van der Pijl L (1982). Principles of Dispersal in Higher Plants 3rd eds. Springer-Verlag, New York, 214.
[34]	van der Wall SB, Kuhn KM, Gworek JR (2005). Two phase seed dispersal: linking the effects of frugivorous birds and seed-caching rodents. Oecologia, 145, 282-287. URL PMID
[35]	van der Wall SB, Longland WS (2004). Diplochory: are two seed dispersers better than one? Trends in Ecology and Evolution, 19, 155-161.
[36]	Wang BC, Smith TB (2002). Closing the seed dispersal loop. Trends in Ecology and Evolution, 17, 379-385.
[37]	Whitmore TC (1984). Tropical Rain Forest of the Far East 2nd edn. Oxford University Press, London.