榕树隐头花序挥发物组成及其传粉榕小蜂寄主识别行为
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摘要
榕树(Ficus spp.)通过挥发性化学物质来吸引传粉榕小蜂(Agaonidae),这种特异性的化学信号释放存在着两种模式,一种是释放多种化合物的"泛化"模式,另一种是释放不常见单一化合物的"专化"模式。为揭示榕树(Ficus microcarpa)及其传粉榕小蜂Eupristina verticillata之间的化学通讯机制,该研究采用固相微萃取法提取榕树隐头花序不同发育期(花前期、雌花期传粉前后、间花期、雄花期和花后期)释放的挥发物,并用气相色谱-质谱联用仪鉴定挥发物成分,分析其变化动态,再通过Y型嗅觉仪检测榕树传粉榕小蜂对各发育期隐头花序的行为反应。结果表明:榕树隐头花序释放的挥发性化合物共鉴定出21种,主要是脂肪酸衍生物、萜类化合物和芳香族化合物。不同发育期隐头花序的挥发物组分差异明显,雌花期传粉前后的挥发物差异表现为传粉后萜类化合物含量下降,脂肪酸衍生物含量增加,特别是传粉前含量较高的特征化合物2-庚酮和3-辛酮消失,D-柠檬烯含量下降,而可巴烯、环己烷和2-己烯醛含量上升。行为检测的结果也表明:雌花期隐头花序对传粉榕小蜂的吸引作用最强,而雄花期的隐头花序释放的挥发物对传粉榕小蜂有趋避作用,形成了对传粉榕小蜂"推拉"的互作模式。有多种化合物在榕树传粉榕小蜂的寄主识别过程中发挥作用,表明榕树及其传粉榕小蜂的互惠共生关系是通过多种化合物的"泛化"策略来维系的。
Aims Chemical communication plays a key role in host plant recognition of pollinators. There are two recognized types of chemical communication between syconia and their pollinating fig wasps: one is "generalization", of which the wasps respond to the relative ratio of multiple compounds, and the other is "specialization", of which the key signal is a single uncommon, possibly unique, compound. The aims of this study were to identify the chemical composition of volatiles from the syconia of Ficus microcarpa at different developmental phases, and to determine if the signaling between F. microcarpa and its pollinating fig wasp, Eupristina verticillata, is of generalized type, or of specialized type.Methods The volatiles from syconia of F.microcarpa were extracted using solid-phase micro extraction(SPME)at different developmental phases(pre-female,female(before and after pollination),interfloral,male and postfloral phases)and the chemical compounds were identified by gas chromatography mass spectrometry(GC-MS).We then tested the behavioral responses of E.verticillata to fresh syconia at different developmental phases using two-choice olfactometers.Important findings There were 21 volatile compounds identified from the syconia at different developmental phases,which were mainly fatty acid derivatives,terpenoids and aromatic compounds.The components of the volatiles apparently differed among the developmental stages.The contents of terpenoids declined,but the contents of fatty acid derivatives increased,from before the pollination to after the pollination.Especially,the characteristic compounds of 2-heptanone and 3-octanone before the pollination disappeared,D-limonene decreased after the pollination,but copanene,cyclohexane and 2-hexenal increased.The results of the two-choice olfactometer experiment showed that the pollinating fig wasps had higher selection ratio to chemicals found in the female phase syconia than those in other phases;whereas the volatile compounds from the male phase syconia had the function pushing the pollinating fig wasps to leave the natal syconia so that there existed the"push-pull"responses by fig wasps to volatiles released by their host syconia.We conclude that there are multiple chemical compounds playing the roles in host recognition of pollinating fig wasp E.verticillata.The mutualistic relationship between F.microcarpa and E.verticillata is maintained by the chemical communication of"generalization"strategy.
Aims Chemical communication plays a key role in host plant recognition of pollinators. There are two recognized types of chemical communication between syconia and their pollinating fig wasps: one is "generalization", of which the wasps respond to the relative ratio of multiple compounds, and the other is "specialization", of which the key signal is a single uncommon, possibly unique, compound. The aims of this study were to identify the chemical composition of volatiles from the syconia of Ficus microcarpa at different developmental phases, and to determine if the signaling between F. microcarpa and its pollinating fig wasp, Eupristina verticillata, is of generalized type, or of specialized type.Methods The volatiles from syconia of F.microcarpa were extracted using solid-phase micro extraction(SPME)at different developmental phases(pre-female,female(before and after pollination),interfloral,male and postfloral phases)and the chemical compounds were identified by gas chromatography mass spectrometry(GC-MS).We then tested the behavioral responses of E.verticillata to fresh syconia at different developmental phases using two-choice olfactometers.Important findings There were 21 volatile compounds identified from the syconia at different developmental phases,which were mainly fatty acid derivatives,terpenoids and aromatic compounds.The components of the volatiles apparently differed among the developmental stages.The contents of terpenoids declined,but the contents of fatty acid derivatives increased,from before the pollination to after the pollination.Especially,the characteristic compounds of 2-heptanone and 3-octanone before the pollination disappeared,D-limonene decreased after the pollination,but copanene,cyclohexane and 2-hexenal increased.The results of the two-choice olfactometer experiment showed that the pollinating fig wasps had higher selection ratio to chemicals found in the female phase syconia than those in other phases;whereas the volatile compounds from the male phase syconia had the function pushing the pollinating fig wasps to leave the natal syconia so that there existed the"push-pull"responses by fig wasps to volatiles released by their host syconia.We conclude that there are multiple chemical compounds playing the roles in host recognition of pollinating fig wasp E.verticillata.The mutualistic relationship between F.microcarpa and E.verticillata is maintained by the chemical communication of"generalization"strategy.
引文
Bronstein JL(1987).Maintenance of species-specificity in a neotropical fig:Pollinator wasp mutualism.Oikos,48,39-46.
Chang XS,Wu CY,Cao ZY(1998).Flora of China 23(1).Science Press,Beijing.112-113.(in Chinese)[张秀实,吴征镒,曹子余(1998).中国植物志第23卷第1分册,科学出版社,北京.112-113.]
Chen C,Song QS,Proffit M,Bessière JM,Li ZB,Hossaert-Mc Key M(2009).Private channel:A single unusual compound assures specific pollinator attraction in Ficus semicordata.Functional Ecology,23,941-950.
Chen YR,Chou LS,Wu WJ(2001).Regulation of fig wasp entry and egress:The role of ostiole of Ficus microcarpa L.Formosan Entomologist,21,171-182.
Cook JM,Segar ST(2010).Speciation in fig wasps.Ecological Entomology,35,54-66.
Cornille A,Underhill JG,Cruaud A,Hossaert-Mc Key M,Johnson SD,Tolley KA,Kjellberg F,van Noort S,Proffit M(2012).Floral volatiles,pollinator sharing and diversification in the fig-wasp mutualism:Insights from Ficus natalensis,and its two wasp pollinators(South Africa).Proceedings of the Royal Society B:Biological Sciences,279,1731-1739.
Cruaud A,R?nsted N,Chantarasuwan B,Chou LS,Clement WL,Couloux A,Cousins B,Genson G,Harrison RD,Hanson PE,Hossaert-Mc Key M,Jabbour-Zahab R,Jousselin E,KerdelhuéC,Kjellberg F,Lopez-Vaamonde C,Peebles J,Peng YQ,Pereira RA,Schramm T,Ubaidillah R,van Noort S,Weiblen GD,Yan DR,Yodpinyanee A,Libeskind-Hadas R,Cook JM,Rasplus JY,Savolainen V(2012).An extreme case of plant-insect codiversification:Figs and fig-pollinating wasps.Systematic Biology,61,1029-1047.
Degenhardt J,Gershenzon J,Baldwin IT,Kessler A(2003).Attracting friends to feast on foes:Engineering terpene emission to make crop plants more attractive to herbivore enemies.Current Opinion in Biotechnology,14,169-176.
D?tterl S,Füssel U,Jürgens A,Aas G(2005).1,4-Dimethoxybenzene,a floral scent compound in willows that attracts an oligolectic bee.Journal of Chemical Ecology,31,2993-2998.
Du JW(2001).Plant-insect behavior and chemical communication and the behavior control.Plant Physiology Communications,27(3),193-200.(in Chinese with English abstract)[杜家纬(2001).植物-昆虫间的化学通讯及其行为控制.植物生理学报,27(3),193-200.]
Dufa?M,Anstett MC(2003).Conflicts between plants and pollinators that reproduce within inflorescences:Evolutionary variations on a theme.Oikos,100,3-14.
Galil J,Eisikowitch D(1968).On the pollination ecology of Ficus sycomorus in East Africa.Ecology,49,259-269.
Geng XZ,Wang B,Jia AQ,Wang RW(2014).Roles of semiochemicals in regulating intraspecific competition of pollinating wasps of Ficus racemosa.Biodiversity Science,22,189-195.(in Chinese with English abstract)[耿向宗,王波,贾爱群,王瑞武(2014).聚果榕小蜂种内竞争的化学信息调节机制初探.生物多样性,22,189-195.]
Grison-PigéL,Edwards AA,Hossaert-Mc Key M(1999).Interspecies variation in floral fragrances emitted by tropical Ficus species.Phytochemistry,52,1293-1299.
Grison-PigéL,Hossaert-Mckey M,Greeff JM,Bessière JM.(2002).Fig volatile compounds-A first comparative study.Phytochemistry,61,61-71.
Gu D,Compton SG,Peng YQ,Yang DR(2012).‘Push’and‘pull’responses by fig wasps to volatiles released by their host figs.Chemoecology,22,217-227.
Harrison RD,Shanahan M(2005).Seventy-seven ways to be a fig:Overview of a diverse plant assemblage.In:Roubik DW,Sakai S,Hamid AA eds.Pollination Ecology and the Rain Forest Canopy:Sarawak Studies.Springer-Verlag,New York.111-127.
Herre EA,Jandér KC,Machado CA(2008).Evolutionary ecology of figs and their associates:Recent progress and outstanding puzzles.Annual Review of Ecology,Evolution,and Systematics,39,439-458.
Hossaert-Mc Key M,Soler C,Schatz B,Proffit M(2010).Floral scents:Their roles in nursery pollination mutualisms.Chemoecology,20,75-88.
Knudsen JT,Tollsten L,Bergstr?m LG(1993).Floral scents-A checklist of volatile compounds isolated by head-space techniques.Phytochemistry,33,253-280.
Kong Y(2014).The Structure and Function of Fig Wasp Community on Ficus microcarpa in Different Locations in Yunnan.Master degree dissertation,Institute of Xishuangbanna Tropical Botanical Garden,Chinese Academy of Sciences,Kunming.13-14.(in Chinese with English abstract)[孔月(2014).云南不同分布区榕树(Ficus microcarpa)果内榕小蜂群落结构和功能的研究.硕士学位论文,中国科学院西双版纳热带植物园,昆明.13-14.]
Li ZB(2010).The Role of Fig Volatiles on the Host Selecting Behavior of the Pollinating Fig Wasps.Ph D dissertation,Institute of Xishuangbanna Tropical Botanical Garden,Chinese Academy of Sciences,Kunming.106-108.(in Chinese with English abstract)[李宗波(2010).榕树隐头果挥发性化合物在传粉小蜂寄主选择过程中的作用.博士学位论文,中国科学院西双版纳热带植物园,昆明.106-108.]
Li ZB,Yang P,Peng YQ,Yang DR(2012).Analysis on chemical compounds and characteristics of fig volatiles emitted from Ficus curtipes Corner.Journal of Tropical and Subtropical Botany,20,292-298.(in Chinese with English abstract)[李宗波,杨培,彭艳琼,杨大荣(2012).钝叶榕隐头果挥发物成分及其构成特征分析,热带亚热带植物学报,20,292-298.]
Liu C,Yang DR,Compton SG,Peng YQ(2013).Larger fig wasps are more careful about which figs to enter--With good reason.PLOS ONE,8,e74117.doi:10.1371/journal.pone.0074117.
Lu RC,Chen JJ,Lin YJ,Wen HF,Shi WJ(2015).The analysis of the volatile commounds which collected from Pelargonium citrosum Van Leenii.Journal of Northwest Forestry University,30,213-216.(in Chinese with English abstract)[路荣春,陈佳佳,林宇杰,闻海峰,施文健(2015).驱蚊草(Pelargonium citrosum Van Leenii)挥发物成分的采集与分析.西北林学院学报,30,213-216.]
Proffit M,Schatz B,Borges RM,Hossaert-Mc Key M(2007).Chemical mediation and niche partitioning in non-pollinating fig-wasp communities.Journal of Animal Ecology,76,296-303.
Proffit M,Schatz B,Bessière JM,Chen C,Soler C,HossaertMc Key M(2008).Signalling receptivity:Comparison of the emission of volatile compounds by figs of Ficus hispida before,during and after the phase of receptivity to pollinators.Symbiosis,45,15-24.
Pellmyr O,Thien LB(1986).Insect reproduction and floral fragrances:Keys to the evolution of the angiosperms?Taxon,35,76-85.
Qin JD,Wang CZ(2001).The relation of interaction between insects and plants to evolution.Acta Entomologica Sinica,44,360-365.(in Chinese with English abstract).[钦俊德,王琛柱(2001).论昆虫与植物的相互作用和进化的关系.昆虫学报,44,360-365.]
R Development Core Team(2015).R:A Language and Environment for Statistical Computing.R Foundation for Statistical Computing,Vienna,Austria.http://www.r-project.org.Cited:2016-06-15.
Sakai S(2002).Aristolochia spp.(Aristolochiaceae)pollinated by flies breeding on decomposing flowers in Panama.American Journal of Botany,89,527-534.
Soler C,Hossaert-Mc Key M,Buatois B,Bessière JM,Schatz B,Proffit M(2011).Geographic variation of floral scent in a highly specialized pollination mutualism.Phytochemistry,72,74-81.
Song QS,Yang DR,Zhang GM,Yang CR(2001).Volatiles from Ficus hispida and their attractiveness to fig wasps.Journal of Chemical Ecology,27,1929-1942.
Verkerke V(1989).Structure and function of the fig.Experientia,45,612-622.
Wang B,Geng XZ,Ma LB,Cook JM,Wang RW(2014).Atrophic cascade induced by predatory ants in a fig-fig wasp mutualism.Journal of Animal Ecology,83,1149-1157.
Wang R,Aylwin R,Louise B,Chen XY,Chen Y,Chou LS,Cobb J,Collette D,Caraine L,Giblin R,Ghana S,Harper M,Harrison R,Mcpherson J,Peng YQ,Pereira R,Reyes A,Rodriguez LJV,Strange E,van Noort S,Yang HW,Yu H,Compton SG(2015).The fig wasp followers and colonists of a widely introduced fig tree,Ficus microcarpa.Insect Conservation&Diversity,8,322-336.
Ware AB,Kaye PT,Compton SG,van Noort S(1993).Fig volatiles:Their role in attracting pollinators and maintaining pollinator specificity.Plant Systematics&Evolution,186,147-156.
Whittaker RH,Feeny PP(1971).Allelochemics:Chemical interactions between species.Science,171,757-770.
Xu ZF,Zhu H,Yang DR(1996).Species diversity and ecological significance of Ficus in tropical rain forest of southern Yunnan Province.In:Chen XW,Zhang YH eds.Collected Research Papers on the Tropical Botany(Ⅳ).Yunnan University Press,Kunming.1-15.(in Chinese)[许再富,朱华,杨大荣(1996).滇南热带雨林榕树类群多样性及生态学意义.见:陈新文,张永宏编.热带植物研究论文报告集,第4集.云南大学出版社,昆明.1-15.]
Zhang KY(1963).A preliminary analysis of the characteristics and formation factors of climate in south Yunnan.Journal of Meteorology,33,218-230.(in Chinese)[张克映(1963).滇南气候的特征及其形成因子的初步分析.气象学报,33,218-230.]
Zhang Y,Yang DR,Peng YQ,Compton SG(2012).Costs of inflorescence longevity for an Asian fig tree and its pollinator.Evolutionary Ecology,26,513-527.
Chang XS,Wu CY,Cao ZY(1998).Flora of China 23(1).Science Press,Beijing.112-113.(in Chinese)[张秀实,吴征镒,曹子余(1998).中国植物志第23卷第1分册,科学出版社,北京.112-113.]
Chen C,Song QS,Proffit M,Bessière JM,Li ZB,Hossaert-Mc Key M(2009).Private channel:A single unusual compound assures specific pollinator attraction in Ficus semicordata.Functional Ecology,23,941-950.
Chen YR,Chou LS,Wu WJ(2001).Regulation of fig wasp entry and egress:The role of ostiole of Ficus microcarpa L.Formosan Entomologist,21,171-182.
Cook JM,Segar ST(2010).Speciation in fig wasps.Ecological Entomology,35,54-66.
Cornille A,Underhill JG,Cruaud A,Hossaert-Mc Key M,Johnson SD,Tolley KA,Kjellberg F,van Noort S,Proffit M(2012).Floral volatiles,pollinator sharing and diversification in the fig-wasp mutualism:Insights from Ficus natalensis,and its two wasp pollinators(South Africa).Proceedings of the Royal Society B:Biological Sciences,279,1731-1739.
Cruaud A,R?nsted N,Chantarasuwan B,Chou LS,Clement WL,Couloux A,Cousins B,Genson G,Harrison RD,Hanson PE,Hossaert-Mc Key M,Jabbour-Zahab R,Jousselin E,KerdelhuéC,Kjellberg F,Lopez-Vaamonde C,Peebles J,Peng YQ,Pereira RA,Schramm T,Ubaidillah R,van Noort S,Weiblen GD,Yan DR,Yodpinyanee A,Libeskind-Hadas R,Cook JM,Rasplus JY,Savolainen V(2012).An extreme case of plant-insect codiversification:Figs and fig-pollinating wasps.Systematic Biology,61,1029-1047.
Degenhardt J,Gershenzon J,Baldwin IT,Kessler A(2003).Attracting friends to feast on foes:Engineering terpene emission to make crop plants more attractive to herbivore enemies.Current Opinion in Biotechnology,14,169-176.
D?tterl S,Füssel U,Jürgens A,Aas G(2005).1,4-Dimethoxybenzene,a floral scent compound in willows that attracts an oligolectic bee.Journal of Chemical Ecology,31,2993-2998.
Du JW(2001).Plant-insect behavior and chemical communication and the behavior control.Plant Physiology Communications,27(3),193-200.(in Chinese with English abstract)[杜家纬(2001).植物-昆虫间的化学通讯及其行为控制.植物生理学报,27(3),193-200.]
Dufa?M,Anstett MC(2003).Conflicts between plants and pollinators that reproduce within inflorescences:Evolutionary variations on a theme.Oikos,100,3-14.
Galil J,Eisikowitch D(1968).On the pollination ecology of Ficus sycomorus in East Africa.Ecology,49,259-269.
Geng XZ,Wang B,Jia AQ,Wang RW(2014).Roles of semiochemicals in regulating intraspecific competition of pollinating wasps of Ficus racemosa.Biodiversity Science,22,189-195.(in Chinese with English abstract)[耿向宗,王波,贾爱群,王瑞武(2014).聚果榕小蜂种内竞争的化学信息调节机制初探.生物多样性,22,189-195.]
Grison-PigéL,Edwards AA,Hossaert-Mc Key M(1999).Interspecies variation in floral fragrances emitted by tropical Ficus species.Phytochemistry,52,1293-1299.
Grison-PigéL,Hossaert-Mckey M,Greeff JM,Bessière JM.(2002).Fig volatile compounds-A first comparative study.Phytochemistry,61,61-71.
Gu D,Compton SG,Peng YQ,Yang DR(2012).‘Push’and‘pull’responses by fig wasps to volatiles released by their host figs.Chemoecology,22,217-227.
Harrison RD,Shanahan M(2005).Seventy-seven ways to be a fig:Overview of a diverse plant assemblage.In:Roubik DW,Sakai S,Hamid AA eds.Pollination Ecology and the Rain Forest Canopy:Sarawak Studies.Springer-Verlag,New York.111-127.
Herre EA,Jandér KC,Machado CA(2008).Evolutionary ecology of figs and their associates:Recent progress and outstanding puzzles.Annual Review of Ecology,Evolution,and Systematics,39,439-458.
Hossaert-Mc Key M,Soler C,Schatz B,Proffit M(2010).Floral scents:Their roles in nursery pollination mutualisms.Chemoecology,20,75-88.
Knudsen JT,Tollsten L,Bergstr?m LG(1993).Floral scents-A checklist of volatile compounds isolated by head-space techniques.Phytochemistry,33,253-280.
Kong Y(2014).The Structure and Function of Fig Wasp Community on Ficus microcarpa in Different Locations in Yunnan.Master degree dissertation,Institute of Xishuangbanna Tropical Botanical Garden,Chinese Academy of Sciences,Kunming.13-14.(in Chinese with English abstract)[孔月(2014).云南不同分布区榕树(Ficus microcarpa)果内榕小蜂群落结构和功能的研究.硕士学位论文,中国科学院西双版纳热带植物园,昆明.13-14.]
Li ZB(2010).The Role of Fig Volatiles on the Host Selecting Behavior of the Pollinating Fig Wasps.Ph D dissertation,Institute of Xishuangbanna Tropical Botanical Garden,Chinese Academy of Sciences,Kunming.106-108.(in Chinese with English abstract)[李宗波(2010).榕树隐头果挥发性化合物在传粉小蜂寄主选择过程中的作用.博士学位论文,中国科学院西双版纳热带植物园,昆明.106-108.]
Li ZB,Yang P,Peng YQ,Yang DR(2012).Analysis on chemical compounds and characteristics of fig volatiles emitted from Ficus curtipes Corner.Journal of Tropical and Subtropical Botany,20,292-298.(in Chinese with English abstract)[李宗波,杨培,彭艳琼,杨大荣(2012).钝叶榕隐头果挥发物成分及其构成特征分析,热带亚热带植物学报,20,292-298.]
Liu C,Yang DR,Compton SG,Peng YQ(2013).Larger fig wasps are more careful about which figs to enter--With good reason.PLOS ONE,8,e74117.doi:10.1371/journal.pone.0074117.
Lu RC,Chen JJ,Lin YJ,Wen HF,Shi WJ(2015).The analysis of the volatile commounds which collected from Pelargonium citrosum Van Leenii.Journal of Northwest Forestry University,30,213-216.(in Chinese with English abstract)[路荣春,陈佳佳,林宇杰,闻海峰,施文健(2015).驱蚊草(Pelargonium citrosum Van Leenii)挥发物成分的采集与分析.西北林学院学报,30,213-216.]
Proffit M,Schatz B,Borges RM,Hossaert-Mc Key M(2007).Chemical mediation and niche partitioning in non-pollinating fig-wasp communities.Journal of Animal Ecology,76,296-303.
Proffit M,Schatz B,Bessière JM,Chen C,Soler C,HossaertMc Key M(2008).Signalling receptivity:Comparison of the emission of volatile compounds by figs of Ficus hispida before,during and after the phase of receptivity to pollinators.Symbiosis,45,15-24.
Pellmyr O,Thien LB(1986).Insect reproduction and floral fragrances:Keys to the evolution of the angiosperms?Taxon,35,76-85.
Qin JD,Wang CZ(2001).The relation of interaction between insects and plants to evolution.Acta Entomologica Sinica,44,360-365.(in Chinese with English abstract).[钦俊德,王琛柱(2001).论昆虫与植物的相互作用和进化的关系.昆虫学报,44,360-365.]
R Development Core Team(2015).R:A Language and Environment for Statistical Computing.R Foundation for Statistical Computing,Vienna,Austria.http://www.r-project.org.Cited:2016-06-15.
Sakai S(2002).Aristolochia spp.(Aristolochiaceae)pollinated by flies breeding on decomposing flowers in Panama.American Journal of Botany,89,527-534.
Soler C,Hossaert-Mc Key M,Buatois B,Bessière JM,Schatz B,Proffit M(2011).Geographic variation of floral scent in a highly specialized pollination mutualism.Phytochemistry,72,74-81.
Song QS,Yang DR,Zhang GM,Yang CR(2001).Volatiles from Ficus hispida and their attractiveness to fig wasps.Journal of Chemical Ecology,27,1929-1942.
Verkerke V(1989).Structure and function of the fig.Experientia,45,612-622.
Wang B,Geng XZ,Ma LB,Cook JM,Wang RW(2014).Atrophic cascade induced by predatory ants in a fig-fig wasp mutualism.Journal of Animal Ecology,83,1149-1157.
Wang R,Aylwin R,Louise B,Chen XY,Chen Y,Chou LS,Cobb J,Collette D,Caraine L,Giblin R,Ghana S,Harper M,Harrison R,Mcpherson J,Peng YQ,Pereira R,Reyes A,Rodriguez LJV,Strange E,van Noort S,Yang HW,Yu H,Compton SG(2015).The fig wasp followers and colonists of a widely introduced fig tree,Ficus microcarpa.Insect Conservation&Diversity,8,322-336.
Ware AB,Kaye PT,Compton SG,van Noort S(1993).Fig volatiles:Their role in attracting pollinators and maintaining pollinator specificity.Plant Systematics&Evolution,186,147-156.
Whittaker RH,Feeny PP(1971).Allelochemics:Chemical interactions between species.Science,171,757-770.
Xu ZF,Zhu H,Yang DR(1996).Species diversity and ecological significance of Ficus in tropical rain forest of southern Yunnan Province.In:Chen XW,Zhang YH eds.Collected Research Papers on the Tropical Botany(Ⅳ).Yunnan University Press,Kunming.1-15.(in Chinese)[许再富,朱华,杨大荣(1996).滇南热带雨林榕树类群多样性及生态学意义.见:陈新文,张永宏编.热带植物研究论文报告集,第4集.云南大学出版社,昆明.1-15.]
Zhang KY(1963).A preliminary analysis of the characteristics and formation factors of climate in south Yunnan.Journal of Meteorology,33,218-230.(in Chinese)[张克映(1963).滇南气候的特征及其形成因子的初步分析.气象学报,33,218-230.]
Zhang Y,Yang DR,Peng YQ,Compton SG(2012).Costs of inflorescence longevity for an Asian fig tree and its pollinator.Evolutionary Ecology,26,513-527.