对叶榕花序不同发育时期气味成分的变化及其对传粉者的吸引作用
|
摘要
为探讨榕果发育过程中气味挥发物的动态变化及其对传粉者行为的调节作用,比较对叶榕(Ficus hispia)不同发育时期花序挥发物的变化,并结合Y形嗅觉仪检测对叶榕传粉榕小蜂对不同花序的选择性。结果表明,在3个发育时期的花序中共检测到64种化合物,对叶榕采用"泛化"策略吸引传粉榕小蜂,十一烷、β-榄香烯、β-芹子烯、α-依兰油烯可能是对传粉榕小蜂起吸引作用的物质。雌前期花序气味与雌花期相似,间花期与雌前期、雌花期的有显著差异,传粉榕小蜂对雌前期和雌花期花序具有明显的选择倾向,对间花期花序表现出驱避性,表明对叶榕与传粉者存在"推-拉"作用模式。雌前期花序释放的气味,有助于传粉者对寄主的定位。同一时期个体间的气味成分存在空间异质性,这种异质性在间花期更加显著,表明气味成分受环境影响。间花期花序气味由于不需要特异性地吸引传粉者,因而更容易发生变化。这有助于更好地理解榕树挥发性物质的组成特点,以及化学机制在维持榕树-榕小蜂共生体系中的关键作用。
In order to understand the changes in volatile organic compounds(VOCs) of figs and its regulation to pollinators, the compositions of VOCs at three floral phases were determined in Ficus hispia, and the behavioral responses of pollinators to different developmental syconia were observed by using Y-tube olfactometer. The results showed that there were 64 compounds were detected in syconia at three phases. Among them, four compounds, such as undecane, β-elemene, β-selinene, and α-muurolene, might be the active substances attractive to pollinators. So the specific chemical signal of F. hispida to attract its pollinator was achieved by"generalization" strategy. The NMDS results showed that the VOCs of syconia at prefemale phase were similar to those at female phase, but those at interfloral phase were significantly different from those at the other two phases.There was a clear tendency for pollinators to select the syconia at prefemale and female phases, but avoid the ones at interfloral phase, indicating that there was a "push-pull" interaction mode between the figs and their pollinators.The VOCs released by syconia at pre-female phase could strengthen pollinator attraction. In addition, the VOCs vary among individuals at the same developmental phase showed VOCs emission was affected by the environment, especially at interfloral phase. These would help for understand the composition characteristics of VOCs in Ficus and the chemical signal function in maintaining fig-fig wasp mutualisms.
In order to understand the changes in volatile organic compounds(VOCs) of figs and its regulation to pollinators, the compositions of VOCs at three floral phases were determined in Ficus hispia, and the behavioral responses of pollinators to different developmental syconia were observed by using Y-tube olfactometer. The results showed that there were 64 compounds were detected in syconia at three phases. Among them, four compounds, such as undecane, β-elemene, β-selinene, and α-muurolene, might be the active substances attractive to pollinators. So the specific chemical signal of F. hispida to attract its pollinator was achieved by"generalization" strategy. The NMDS results showed that the VOCs of syconia at prefemale phase were similar to those at female phase, but those at interfloral phase were significantly different from those at the other two phases.There was a clear tendency for pollinators to select the syconia at prefemale and female phases, but avoid the ones at interfloral phase, indicating that there was a "push-pull" interaction mode between the figs and their pollinators.The VOCs released by syconia at pre-female phase could strengthen pollinator attraction. In addition, the VOCs vary among individuals at the same developmental phase showed VOCs emission was affected by the environment, especially at interfloral phase. These would help for understand the composition characteristics of VOCs in Ficus and the chemical signal function in maintaining fig-fig wasp mutualisms.
引文
[1]BERG C C.Classification and distribution of Ficus[J].Experientia,1989,45(7):605-611.doi:10.1007/BF01975677.
[2]JANZEN D H.How to be a fig[J].Annu Rev Ecol Syst,1979,10:13-51.doi:10.1146/annurev.es.10.110179.000305.
[3]COOK J M,RASPLUS J Y.Mutualists with attitude:Coevolving fig wasps and figs[J].Trends Ecol Evol,2003,18(5):241-248.doi:10.1016/S0169-5347(03)00062-4.
[4]WEIBLEN G D.Phylogenetic relationships of functionally dioecious Ficus(Moraceae)based on ribosomal DNA sequences and morphology[J].Amer J Bot,2000,87(9):1342-1357.doi:10.2307/2656726.
[5]PROFFIT M,JOHNSON S D.Specificity of the signal emitted by figs to attract their pollinating wasps:Comparison of volatile organic compounds emitted by receptive syconia of Ficus sur and F.sycomorus in southern Africa[J].S Afr J Bot,2009,75(4):771-777.doi:10.1016/j.sajb.2009.08.006.
[6]HOSSAERT-MCKEY M,GIBERNAU M,FREY J E.Chemosensory attraction of fig wasps to substances produced by receptive figs[J].Entomol Exp Appl,1994,70(2):185-191.doi:10.1111/j.1570-7458.1994.tb00746.x.
[7]HOSSAERT-MCKEY M,SOLER C,SCHATZ B,et al.Floral scents:Their roles in nursery pollination mutualisms[J].Chemoecology,2010,20(2):75-88.doi:10.1007/s00049-010-0043-5.
[8]DUDAREVA N,NEGRE F.Practical applications of research into the regulation of plant volatile emission[J].Curr Opin Plant Biol,2005,8(1):113-118.doi:10.1016/j.pbi.2004.11.007.
[9]KNUDSEN J T,ERIKSSON R,GERSHENZON J,et al.Diversity and distribution of floral scent[J].Bot Rev,2006,72(1):1-120.doi:10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2.
[10]F?GRI K,van DER P L.The Principles of Pollination Ecology[M].3rd ed.Oxford,New York:Pergamon Press,1979:1.
[11]PICHERSKY E,GERSHENZON J.The formation and function of plant volatiles:Perfumes for pollinator attraction and defense[J].Curr Opin Plant Biol,2002,5(3):237-243.doi:10.1016/S1369-5266(02)00251-0.
[12]WEIBLEN G D.How to be a fig waps[J].Annu Rev Entomol,2002,47:299-330.
[13]SAKAI S.Aristolochia spp.(Aristolochiaceae)pollinated by flies breeding on decomposing flowers in Panama[J].Amer J Bot,2002,89(3):527-534.doi:10.3732/ajb.89.3.527.
[14]GRISON-PIGéL,BESSIèRE J M,HOSSAERT-MCKEY M.Specific attraction of fig-pollinating wasps:Role of volatile compounds released by tropical figs[J].J Chem Ecol,2002,28(2):283-295.doi:10.1023/A:1017930023741.
[15]CHEN C,SONG Q S,PROFFIT M,et al.Private channel:A single unusual compound assures specific pollinator attraction in Ficus semicordata[J].Funct Ecol,2009,23(5):941-950.doi:10.1111/j.1365-2435.2009.01622.x.
[16]GALIL J,EISIKOWITCH D.On the pollination ecology of Ficus sycomorus in East Africa[J].Ecology,1968,49(2):259-269.doi:10.2307/1934454.
[17]CORNER E J H.Check-list of Ficus in Asia and Australasia with keys to identification[J].Gard Bull Singap,1965,21:1-186.
[18]SOLER C,HOSSAERT-MCKEY M,BUATOIS B,et al.Geographic variation of floral scent in a highly specialized pollination mutualism[J].Phytochemistry,2011,72:74-81.
[19]ZHANG T,WANG B,MIAO B G,et al.Chemical composition of volatiles from the syconia of Ficus microcarpa and host recognition behavior of pollinating fig wasps[J].Chin J Plant Ecol,2017,41(5):549-558.doi:10.17521/cjpe.2016.0250.张亭,王波,苗白鸽,等.榕树隐头花序挥发物组成及其传粉榕小蜂寄主识别行为[J].植物生态学报,2017,41(5):549-558.doi:10.17521/cjpe.2016.0250.
[20]PROFFIT M,SCHATZ B,BESSIERE J M,et al.Signalling receptivity:Comparison of the emission of volatile compounds by figs of Ficus hispida before,during and after the phase of receptivity to pollinators[J].Symbiosis,2008,45(1/2/3):15-24.
[21]MAYR G L.Neue feigen-insekten[J].Wien Entomol Ztg,1906,25:153-187.
[22]YAN X,PENG Y Q,YANG D R.Spatial distribution patterns of three fig wasps on Ficus semicordata:How non-pollinators affect pollinator’s sex ratio[J].Acta Ecol Sin,2012,32(2):99-103.doi:10.1016/j.chnaes.2012.02.003.
[23]BIANCHI F,CARERI M,MANGIA A,et al.Retention indices in the analysis of food aroma volatile compounds in temperature-programmed gas chromatography:Database creation and evaluation of precision and robustness[J].J Sep Sci,2007,30(4):563-572.doi:10.1002/jssc.200600393.
[24]SONG Q S,YANG D R,ZHANG G M,et al.Volatiles from Ficus hispida and their attractiveness to fig wasps[J].J Chem Ecol,2001,27(10):1929-1942.doi:10.1023/A:1012226400586.
[25]BARKER N P.Evidence of a volatile attractant in Ficus ingens(Moraceae)[J].Bothalia,1985,15(3/4):607-611.doi:10.4102/abc.v15i3/4.1854.
[26]SOLER C,HOSSAERT-MCKEY M,BUATOIS B,et al.Geographic variation of floral scent in a highly specialized pollination mutualism[J].Phytochemistry,2011,72(1):74-81.doi:10.1016/j.phytochem.2010.10.012.
[27]PROFFIT M,SCHATZ B,BORGES R M,et al.Chemical mediation and niche partitioning in non-pollinating fig-wasp communities[J].J Anim Ecol,2007,76(2):296-303.doi:10.1111/j.1365-2656.2007.01213.x.
[28]WILLIAM R B.Coevolution of Ficus and Agaonidae[J].Ann Miss Bot Gard,1974,61(3):770-780.doi:10.2307/2395028.
[29]LIU C,YANG D R,COMPTON S G,et al.Larger fig wasps are more careful about which figs to enter-with good reason[J].PLoS One,2013,8(9):e74117.doi:10.1371/journal.pone.0074117.
[30]SCHIESTL F P,AYASSE M.Post-pollination emission of a repellent compound in a sexually deceptive orchid:A new mechanism for maximising reproductive success?[J].Oecologia,2001,126(4):531-534.doi:10.1007/s004420000552.
[31]TOLLSTEN L.A multivariate approach to post-pollination changes in the floral scent of Platanthera bifolia(Orchidaceae)[J].Nord J Bot,1993,13(5):495-499.
[32]GU D,COMPTON S G,PENG Y Q,et al.‘Push’and‘pull’responses by fig wasps to volatiles released by their host figs[J].Chemoecology,2012,22(4):217-227.doi:10.1007/s00049-012-0108-8.
[33]WANG G,COMPTON S G,CHEN J.The mechanism of pollinator specificity between two sympatric fig varieties:A combination of olfactory signals and contact cues[J].Ann Bot,2013,111(2):173-181.doi:10.1093/aob/mcs250.
[34]MAJETIC C J,RAGUSO R A,ASHMAN T L.Sources of floral scent variation[J].Plant Sign Behav,2009,4(2):129-131.doi:10.4161/psb.4.2.7628.
[2]JANZEN D H.How to be a fig[J].Annu Rev Ecol Syst,1979,10:13-51.doi:10.1146/annurev.es.10.110179.000305.
[3]COOK J M,RASPLUS J Y.Mutualists with attitude:Coevolving fig wasps and figs[J].Trends Ecol Evol,2003,18(5):241-248.doi:10.1016/S0169-5347(03)00062-4.
[4]WEIBLEN G D.Phylogenetic relationships of functionally dioecious Ficus(Moraceae)based on ribosomal DNA sequences and morphology[J].Amer J Bot,2000,87(9):1342-1357.doi:10.2307/2656726.
[5]PROFFIT M,JOHNSON S D.Specificity of the signal emitted by figs to attract their pollinating wasps:Comparison of volatile organic compounds emitted by receptive syconia of Ficus sur and F.sycomorus in southern Africa[J].S Afr J Bot,2009,75(4):771-777.doi:10.1016/j.sajb.2009.08.006.
[6]HOSSAERT-MCKEY M,GIBERNAU M,FREY J E.Chemosensory attraction of fig wasps to substances produced by receptive figs[J].Entomol Exp Appl,1994,70(2):185-191.doi:10.1111/j.1570-7458.1994.tb00746.x.
[7]HOSSAERT-MCKEY M,SOLER C,SCHATZ B,et al.Floral scents:Their roles in nursery pollination mutualisms[J].Chemoecology,2010,20(2):75-88.doi:10.1007/s00049-010-0043-5.
[8]DUDAREVA N,NEGRE F.Practical applications of research into the regulation of plant volatile emission[J].Curr Opin Plant Biol,2005,8(1):113-118.doi:10.1016/j.pbi.2004.11.007.
[9]KNUDSEN J T,ERIKSSON R,GERSHENZON J,et al.Diversity and distribution of floral scent[J].Bot Rev,2006,72(1):1-120.doi:10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2.
[10]F?GRI K,van DER P L.The Principles of Pollination Ecology[M].3rd ed.Oxford,New York:Pergamon Press,1979:1.
[11]PICHERSKY E,GERSHENZON J.The formation and function of plant volatiles:Perfumes for pollinator attraction and defense[J].Curr Opin Plant Biol,2002,5(3):237-243.doi:10.1016/S1369-5266(02)00251-0.
[12]WEIBLEN G D.How to be a fig waps[J].Annu Rev Entomol,2002,47:299-330.
[13]SAKAI S.Aristolochia spp.(Aristolochiaceae)pollinated by flies breeding on decomposing flowers in Panama[J].Amer J Bot,2002,89(3):527-534.doi:10.3732/ajb.89.3.527.
[14]GRISON-PIGéL,BESSIèRE J M,HOSSAERT-MCKEY M.Specific attraction of fig-pollinating wasps:Role of volatile compounds released by tropical figs[J].J Chem Ecol,2002,28(2):283-295.doi:10.1023/A:1017930023741.
[15]CHEN C,SONG Q S,PROFFIT M,et al.Private channel:A single unusual compound assures specific pollinator attraction in Ficus semicordata[J].Funct Ecol,2009,23(5):941-950.doi:10.1111/j.1365-2435.2009.01622.x.
[16]GALIL J,EISIKOWITCH D.On the pollination ecology of Ficus sycomorus in East Africa[J].Ecology,1968,49(2):259-269.doi:10.2307/1934454.
[17]CORNER E J H.Check-list of Ficus in Asia and Australasia with keys to identification[J].Gard Bull Singap,1965,21:1-186.
[18]SOLER C,HOSSAERT-MCKEY M,BUATOIS B,et al.Geographic variation of floral scent in a highly specialized pollination mutualism[J].Phytochemistry,2011,72:74-81.
[19]ZHANG T,WANG B,MIAO B G,et al.Chemical composition of volatiles from the syconia of Ficus microcarpa and host recognition behavior of pollinating fig wasps[J].Chin J Plant Ecol,2017,41(5):549-558.doi:10.17521/cjpe.2016.0250.张亭,王波,苗白鸽,等.榕树隐头花序挥发物组成及其传粉榕小蜂寄主识别行为[J].植物生态学报,2017,41(5):549-558.doi:10.17521/cjpe.2016.0250.
[20]PROFFIT M,SCHATZ B,BESSIERE J M,et al.Signalling receptivity:Comparison of the emission of volatile compounds by figs of Ficus hispida before,during and after the phase of receptivity to pollinators[J].Symbiosis,2008,45(1/2/3):15-24.
[21]MAYR G L.Neue feigen-insekten[J].Wien Entomol Ztg,1906,25:153-187.
[22]YAN X,PENG Y Q,YANG D R.Spatial distribution patterns of three fig wasps on Ficus semicordata:How non-pollinators affect pollinator’s sex ratio[J].Acta Ecol Sin,2012,32(2):99-103.doi:10.1016/j.chnaes.2012.02.003.
[23]BIANCHI F,CARERI M,MANGIA A,et al.Retention indices in the analysis of food aroma volatile compounds in temperature-programmed gas chromatography:Database creation and evaluation of precision and robustness[J].J Sep Sci,2007,30(4):563-572.doi:10.1002/jssc.200600393.
[24]SONG Q S,YANG D R,ZHANG G M,et al.Volatiles from Ficus hispida and their attractiveness to fig wasps[J].J Chem Ecol,2001,27(10):1929-1942.doi:10.1023/A:1012226400586.
[25]BARKER N P.Evidence of a volatile attractant in Ficus ingens(Moraceae)[J].Bothalia,1985,15(3/4):607-611.doi:10.4102/abc.v15i3/4.1854.
[26]SOLER C,HOSSAERT-MCKEY M,BUATOIS B,et al.Geographic variation of floral scent in a highly specialized pollination mutualism[J].Phytochemistry,2011,72(1):74-81.doi:10.1016/j.phytochem.2010.10.012.
[27]PROFFIT M,SCHATZ B,BORGES R M,et al.Chemical mediation and niche partitioning in non-pollinating fig-wasp communities[J].J Anim Ecol,2007,76(2):296-303.doi:10.1111/j.1365-2656.2007.01213.x.
[28]WILLIAM R B.Coevolution of Ficus and Agaonidae[J].Ann Miss Bot Gard,1974,61(3):770-780.doi:10.2307/2395028.
[29]LIU C,YANG D R,COMPTON S G,et al.Larger fig wasps are more careful about which figs to enter-with good reason[J].PLoS One,2013,8(9):e74117.doi:10.1371/journal.pone.0074117.
[30]SCHIESTL F P,AYASSE M.Post-pollination emission of a repellent compound in a sexually deceptive orchid:A new mechanism for maximising reproductive success?[J].Oecologia,2001,126(4):531-534.doi:10.1007/s004420000552.
[31]TOLLSTEN L.A multivariate approach to post-pollination changes in the floral scent of Platanthera bifolia(Orchidaceae)[J].Nord J Bot,1993,13(5):495-499.
[32]GU D,COMPTON S G,PENG Y Q,et al.‘Push’and‘pull’responses by fig wasps to volatiles released by their host figs[J].Chemoecology,2012,22(4):217-227.doi:10.1007/s00049-012-0108-8.
[33]WANG G,COMPTON S G,CHEN J.The mechanism of pollinator specificity between two sympatric fig varieties:A combination of olfactory signals and contact cues[J].Ann Bot,2013,111(2):173-181.doi:10.1093/aob/mcs250.
[34]MAJETIC C J,RAGUSO R A,ASHMAN T L.Sources of floral scent variation[J].Plant Sign Behav,2009,4(2):129-131.doi:10.4161/psb.4.2.7628.