花蜜中酚类物质对群落中同花期植物传粉的影响
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摘要
显花植物分泌花蜜以奖励传粉昆虫为其提供的传粉服务。许多植物分泌的花蜜中除了糖和氨基酸等物质外,还含有与植物抗虫有关的次生代谢物质,如生物碱和多酚。饲喂试验表明传粉蜂类偏爱采集含有这些次生代谢物质的花蜜。因此,花蜜中的次生代谢物质对分泌这类花蜜的植物传粉具有进化和生态上的意义。但是,花蜜中的次生代谢物质是否会影响群落中其它同花期植物的传粉尚不清楚。在2009年3—5月份,在西双版纳永久样地就中华蜜蜂(Apis cerana)的传粉行为进行研究,比较了两种饲喂条件下,整个蜂群采集花蜜的花粉种类和单个采集蜂携带的花粉团的花粉种类,以及采集蜂蜜囊中花蜜的含糖量(一组饲喂30%蔗糖糖浆,以下简称"喂纯糖浆组"另一组饲喂同样糖浆但含有0.01%槲皮素,以下简称"喂酚糖浆组")。研究结果表明:饲喂两种不同糖浆的蜂群拜访的植物种类数量上没有明显差异。但是,两组采集工蜂所选择采集植物花粉种类却存在明显差异,它们采集的花粉都包含了一些特有的花粉种类。另外,两组采集工蜂所采集含有2种以上花粉种类花粉团的蜜蜂数量存在明显差异,喂酚糖浆组明显高于饲喂纯糖浆组。两组工蜂蜜囊中花蜜的含糖量也存在显著差异,喂酚糖浆组工蜂蜜囊中花蜜的含糖量明显高于喂纯糖浆组。因此,喂酚糖浆组的工蜂拜访植物的专一性比较低,在一次采集过程中倾向拜访花蜜中含糖量高的植物。花蜜中酚类物质增加了群落中同花期植物之间的花粉传播,从而降低了整个群落的传粉效率。
Floral nectar provides crucial energy sources for diverse animals,many flowering species produce nectar to reward flower visitors,which provide pollination services for flowering plants.In addition to sugars and amino acids,the nectar of many plant species often contains secondary compounds such as alkaloids and phenolics,which are associated with plant defense against herbivores.The composition of nectar may influence an entire assemblage of local visitors and animal-pollinated plants,but the basis for nectar resource selection is complex.Species co-existence and community assembly mechanisms depend on links between consumers and resources.A previous feeding trial showed that a sugar solution can motivate honey bees to use nectar containing plant defense chemicals(toxic nectar).Toxic-nectar plants are thus expected to be tightly linked with other non-toxic or less toxic floral resources for sharing pollinators,while general impacts of toxic nectar on plant communities have been little investigated.Most previous studies of the ecological and evolutionary significance of nectar secondary compounds have focused on the benefits to the plants that produce these compounds.For example,feeding experiments have shown that honey bees prefer to collect nectar containing secondary compounds.However,few studies have attempted to evaluate the effects of nectar secondary compounds on other co-flowering species in a natural community,so their impact on other synchronously flowering species is still unclear.We conducted a field trial with the Chinese honeybee species Apis cerana in a permanent plot at Xishuangbanna from March to May 2009.We compared the flowering species visited,at the entire colony and individual foraging bee levels,between colonies fed 30% sucrose syrup(hereafter 'S-fed') and the same syrup containing 0.01% quercetin(hereafter 'P-fed').The nectar sugar concentration was also compared between the two treatments.The main results were as follows:(1)At the colony level,although the number of flowering species visited by an entire colony did not differ between the two treatments,the flowering species visited was significantly different between the treatments.Of the 96 species visited,43 were visited by P-fed bees,whereas 17 were visited by S-fed bees.Thirty-six species(about 30% of the total number) were visited by both P-and S-fed bees.(2)At the individual bee level,the number of bees from the P-fed colonies that collected pollen from more than two flowering species was significantly higher than that for bees from S-fed colonies.Thus the number of flowering species selected by individual bees also differed between the treatments.P-fed bees tended to visit more than one species in a single foraging trip,whereas S-fed bees usually foraged on one species only.(3)Compared to S-fed bees,P-fed bees tended to visit the species with nectar containing high concentrations of sugar. Collectively,these results indicate nectar phenolic compounds may reduce pollination efficiency through an indirect impact on bees′ specialization on a given flowering species in a single foraging trip,and phenolic alter bee foraging;bee niche breadth increases dramatically,pollination of rare species may increase,interspecific pollen transfer at flowers may also be affected.
Floral nectar provides crucial energy sources for diverse animals,many flowering species produce nectar to reward flower visitors,which provide pollination services for flowering plants.In addition to sugars and amino acids,the nectar of many plant species often contains secondary compounds such as alkaloids and phenolics,which are associated with plant defense against herbivores.The composition of nectar may influence an entire assemblage of local visitors and animal-pollinated plants,but the basis for nectar resource selection is complex.Species co-existence and community assembly mechanisms depend on links between consumers and resources.A previous feeding trial showed that a sugar solution can motivate honey bees to use nectar containing plant defense chemicals(toxic nectar).Toxic-nectar plants are thus expected to be tightly linked with other non-toxic or less toxic floral resources for sharing pollinators,while general impacts of toxic nectar on plant communities have been little investigated.Most previous studies of the ecological and evolutionary significance of nectar secondary compounds have focused on the benefits to the plants that produce these compounds.For example,feeding experiments have shown that honey bees prefer to collect nectar containing secondary compounds.However,few studies have attempted to evaluate the effects of nectar secondary compounds on other co-flowering species in a natural community,so their impact on other synchronously flowering species is still unclear.We conducted a field trial with the Chinese honeybee species Apis cerana in a permanent plot at Xishuangbanna from March to May 2009.We compared the flowering species visited,at the entire colony and individual foraging bee levels,between colonies fed 30% sucrose syrup(hereafter 'S-fed') and the same syrup containing 0.01% quercetin(hereafter 'P-fed').The nectar sugar concentration was also compared between the two treatments.The main results were as follows:(1)At the colony level,although the number of flowering species visited by an entire colony did not differ between the two treatments,the flowering species visited was significantly different between the treatments.Of the 96 species visited,43 were visited by P-fed bees,whereas 17 were visited by S-fed bees.Thirty-six species(about 30% of the total number) were visited by both P-and S-fed bees.(2)At the individual bee level,the number of bees from the P-fed colonies that collected pollen from more than two flowering species was significantly higher than that for bees from S-fed colonies.Thus the number of flowering species selected by individual bees also differed between the treatments.P-fed bees tended to visit more than one species in a single foraging trip,whereas S-fed bees usually foraged on one species only.(3)Compared to S-fed bees,P-fed bees tended to visit the species with nectar containing high concentrations of sugar. Collectively,these results indicate nectar phenolic compounds may reduce pollination efficiency through an indirect impact on bees′ specialization on a given flowering species in a single foraging trip,and phenolic alter bee foraging;bee niche breadth increases dramatically,pollination of rare species may increase,interspecific pollen transfer at flowers may also be affected.
引文
[1]Elias T S,Bentley B.The Biology of Nectaries.New York:Columbia University Press,1983:126.
[2]Baker H G.Non-sugar chemical constituents of nectar.Apidologie,1977,8(4):349-356.
[3]Adler L S.The ecological significance of toxic nectar.Oikos,2000,91(3):409-420.
[4]Nicholson S W,Thornburg R.Nectsries and Nectar.Dordrecht:Springer-Verlag,2007:215-264.
[5]Baker H G,Baker I.Amino-acids in nectar and their evolutionary significance.Nature,1973,241(5391):543-545.
[6]Faegri K,van der Pijl L.The Principles of Pollination Ecology.Oxford:Pergamon Press,1979:67.
[7]Ohashi K,Natori S,Kubo T.Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of theworker honeybee(Apis mellifera L.).European Journal of Biochemistry,1999,265(1):127-133.
[8]Liu F L,He J Z,Fu W J.Highly controlled nest homeostasis of honey bees helps deactivate phenolics in nectar.Naturwissenschaften,2005,92(6):297-299.
[9]Baker H G,Baker I.Studies of nectar-constitution and pollinator-plant coevolution//Gilbert L E,Raven P H,eds.Coevolution of Animals andPlants.Austin:University of Texas Press,1975:100-140.
[10]Hagler J R,Buchmann S L.Honey bee(Hymenoptera:Apidae)foraging responses to phenolic-rich nectars.Journal of the Kansas EntomologicalSociety,1993,66(2):223-230.
[11]Singaravelan N,Nee'man G,Inbar M,Izhaki I.Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars.Journal of Chemical Ecology,2005,31(12):2791-2804.
[12]Liu F,Chen J,Chai J,Zhang X,Bai X,He D,Roubik D W.Adaptive functions of defensive plant phenolics and a non-linear bee response tonectar components.Functional Ecology,2007,21(1):96-100.
[13]Kretschmar J A,Baumann T W.Caffeine in Citrus flowers.Phytochemistry,1999,52(1):19-23.
[14]London-Shafir I,Shafir S,Eisikowitch D.Amygdalin in almond nectar and pollen-facts and possible roles.Plant Systematics and Evolution,2003,238(1/4):87-95.
[15]Tan K,Guo Y H,Nicolson S W,Radloff S E,Song Q S,Hepburn H R.Honeybee(Apis cerana)foraging responses to the toxic honey ofTripterygium hypoglaucum(Celastraceae):changing threshold of nectar acceptability.Journal of Chemical Ecology,2007,33(12):2209-2217.
[16]Irwin R E,Adler L S.Nectar secondary compounds affect self-pollen transfer:implications for female and male reproduction.Ecology,2008,89(8):2207-2217.
[17]Gegear R J,Manson J S,Thomson J D.Ecological context influences pollinator deterrence by alkaloids in floral nectar.Ecology Letters,2007,10(5):375-382.
[18]Mitchell B K,Sutcliffe J F.Sensory inhibition as a mechanism of feeding deterrence:effects of three alkaloids on leaf beetle feeding.Physiological Entomology,1984,9(1):57-64.
[19]Dethier V G,Bowdan E.The effect of alkaloids on sugar receptors and the feeding behaviour of the blowfly.Physiological Entomology,1989,14(2):127-136.
[20]Glendinning J I.How do herbivorous insects cope with noxious secondary plant compounds in their dietEntomologia Experimentalis et Applicata,2002,104(1):15-25.
[21]Ish-Am G,Eisikowitch D.The behaviour of honey bees(Apis mellifera)visiting avocado(Persea americana)flowers and their contribution to its pollination.Journal of Apicultural Research,1993,32(3/4):175-186.
[22]Ish-Am G,Eisikowitch D.Low attractiveness of avocado(Persea americana Mill.)flowers to honeybees(Apis mellifera L.)limits fruit set in Israel.Journal of Horticultural Science and Biotechnology,1998,73(2):195-204.
[23]Xue J Y,Tang J W,Sha L Q,Meng Y.Soil nutrient contents and their characteristics of seasonal changes under shorea chinensis forest in Xishuangbanna.Acta Phytoecologica Sinica,2003,27(3):373-379.
[24]Cao M,Zou X M,Warren M,Zhu H.Tropical forests of Xishuangbanna,China.Biotropica,2006,38(3):306-309.
[25]Zhu H.Forest vegetation of Xishuangbanna,south China.Forestry Studies in China,2006,8(2):1-58.
[26]Lan G Y,Hu Y H,Cao M,Zhu H,Wang H,Zhou S S,Deng X B,Cui J Y,Huang J G,Liu L Y,Xu H L,Song J P,He Y C.Establishment of xishuangbanna tropical forest dynamics plot:species compositions and spatial distribution patterns.Journal of Plant Ecology,2008,32(2):287-298.
[27]Yao L H,Jiang Y M,Singanusong R,Datta N,Raymont K.Phenolic acids in Australian Melaleuca,Guioa,Lophostemon,Banksia and Helianthus honeys and their potential for floral authentication.Food Research International,2005,38(6):651-658.
[28]Penuelas J,Castells E,Joffre R,Tognetti R.Carbon-based secondary and structural compounds in Mediterranean shrubs growing near a natural CO 2 spring.Global Change Biology,2002,8(3):281-288.
[29]Rossi A M,Stiling P,Moon D C,Cattell M V,Drake B G.Induced defensive response of myrtle oak to foliar insect herbivory in ambient and elevated CO 2.Journal of Chemical Ecology,2004,30(6):1143-1152.
[30]Chen F J,Wu G,Ge F,Parajulee M N,Shrestha R B.Effects of elevated CO 2 and transgenic Bt cotton on plant chemistry,performance,and feeding of an insect herbivore,the cotton bollworm.Entomologia Experimentalis et Applicata,2005,115(2):341-350.
[31]Coley P D,Massa M,Lovelock C E,Winter K.Effects of elevated CO 2 on foliar chemistry of saplings of nine species of tropical tree.Oecologia,2002,133(1):62-69.
[32]Qin J D,Wang C Z.The relation of interaction between insects and plants to evolution.Acta Entomologica Sinica,2001,44(3):360-365.
[33]Potts S G,Vulliamy B,Dafni A,Ne'eman G,Willmer P.Linking bees and flowers:How do floral communities structure pollinator communitiesEcology,2003,84(10):2628-2642.
[34]Kleijn D,Raemakers I.A retrospective analysis of pollen host plant use by stable and declining bumble bee species.Ecology,2008,89(7):1811-1823.
[35]Liu F L,Zhang X W,Chai J P,Yang D R.Pollen phenolics and regulation of pollen foraging in honeybee colony.Behavioral Ecology and Sociobiology,2006,59(4):582-588.
[36]Kessler D,Gase K,Baldwin I T.Field experiments with transformed plants reveal the sense of floral scents.Science,2008,321(5893):1200-1202.
[37]Rhoades D F,Bergdahl J C.Adaptive significance of toxic nectar.The American Naturalist,1981,117(5):798-803.
[23]薛敬意,唐建维,沙丽清,孟盈.西双版纳望天树林土壤养分含量及其季节变化.植物生态学报,2003,27(3):373-379.
[26]兰国玉,胡跃华,曹敏,朱华,王洪,周仕顺,邓晓保,崔景云,黄建国,刘林云,许海龙,宋军平,何有才.西双版纳热带森林动态监测样地——树种组成与空间分布格局.植物生态学报,2008,32(2):287-298.
[32]钦俊德,王琛柱.论昆虫与植物的相互作用和进化的关系.昆虫学报,2001,44(3):360-365.
[2]Baker H G.Non-sugar chemical constituents of nectar.Apidologie,1977,8(4):349-356.
[3]Adler L S.The ecological significance of toxic nectar.Oikos,2000,91(3):409-420.
[4]Nicholson S W,Thornburg R.Nectsries and Nectar.Dordrecht:Springer-Verlag,2007:215-264.
[5]Baker H G,Baker I.Amino-acids in nectar and their evolutionary significance.Nature,1973,241(5391):543-545.
[6]Faegri K,van der Pijl L.The Principles of Pollination Ecology.Oxford:Pergamon Press,1979:67.
[7]Ohashi K,Natori S,Kubo T.Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of theworker honeybee(Apis mellifera L.).European Journal of Biochemistry,1999,265(1):127-133.
[8]Liu F L,He J Z,Fu W J.Highly controlled nest homeostasis of honey bees helps deactivate phenolics in nectar.Naturwissenschaften,2005,92(6):297-299.
[9]Baker H G,Baker I.Studies of nectar-constitution and pollinator-plant coevolution//Gilbert L E,Raven P H,eds.Coevolution of Animals andPlants.Austin:University of Texas Press,1975:100-140.
[10]Hagler J R,Buchmann S L.Honey bee(Hymenoptera:Apidae)foraging responses to phenolic-rich nectars.Journal of the Kansas EntomologicalSociety,1993,66(2):223-230.
[11]Singaravelan N,Nee'man G,Inbar M,Izhaki I.Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars.Journal of Chemical Ecology,2005,31(12):2791-2804.
[12]Liu F,Chen J,Chai J,Zhang X,Bai X,He D,Roubik D W.Adaptive functions of defensive plant phenolics and a non-linear bee response tonectar components.Functional Ecology,2007,21(1):96-100.
[13]Kretschmar J A,Baumann T W.Caffeine in Citrus flowers.Phytochemistry,1999,52(1):19-23.
[14]London-Shafir I,Shafir S,Eisikowitch D.Amygdalin in almond nectar and pollen-facts and possible roles.Plant Systematics and Evolution,2003,238(1/4):87-95.
[15]Tan K,Guo Y H,Nicolson S W,Radloff S E,Song Q S,Hepburn H R.Honeybee(Apis cerana)foraging responses to the toxic honey ofTripterygium hypoglaucum(Celastraceae):changing threshold of nectar acceptability.Journal of Chemical Ecology,2007,33(12):2209-2217.
[16]Irwin R E,Adler L S.Nectar secondary compounds affect self-pollen transfer:implications for female and male reproduction.Ecology,2008,89(8):2207-2217.
[17]Gegear R J,Manson J S,Thomson J D.Ecological context influences pollinator deterrence by alkaloids in floral nectar.Ecology Letters,2007,10(5):375-382.
[18]Mitchell B K,Sutcliffe J F.Sensory inhibition as a mechanism of feeding deterrence:effects of three alkaloids on leaf beetle feeding.Physiological Entomology,1984,9(1):57-64.
[19]Dethier V G,Bowdan E.The effect of alkaloids on sugar receptors and the feeding behaviour of the blowfly.Physiological Entomology,1989,14(2):127-136.
[20]Glendinning J I.How do herbivorous insects cope with noxious secondary plant compounds in their dietEntomologia Experimentalis et Applicata,2002,104(1):15-25.
[21]Ish-Am G,Eisikowitch D.The behaviour of honey bees(Apis mellifera)visiting avocado(Persea americana)flowers and their contribution to its pollination.Journal of Apicultural Research,1993,32(3/4):175-186.
[22]Ish-Am G,Eisikowitch D.Low attractiveness of avocado(Persea americana Mill.)flowers to honeybees(Apis mellifera L.)limits fruit set in Israel.Journal of Horticultural Science and Biotechnology,1998,73(2):195-204.
[23]Xue J Y,Tang J W,Sha L Q,Meng Y.Soil nutrient contents and their characteristics of seasonal changes under shorea chinensis forest in Xishuangbanna.Acta Phytoecologica Sinica,2003,27(3):373-379.
[24]Cao M,Zou X M,Warren M,Zhu H.Tropical forests of Xishuangbanna,China.Biotropica,2006,38(3):306-309.
[25]Zhu H.Forest vegetation of Xishuangbanna,south China.Forestry Studies in China,2006,8(2):1-58.
[26]Lan G Y,Hu Y H,Cao M,Zhu H,Wang H,Zhou S S,Deng X B,Cui J Y,Huang J G,Liu L Y,Xu H L,Song J P,He Y C.Establishment of xishuangbanna tropical forest dynamics plot:species compositions and spatial distribution patterns.Journal of Plant Ecology,2008,32(2):287-298.
[27]Yao L H,Jiang Y M,Singanusong R,Datta N,Raymont K.Phenolic acids in Australian Melaleuca,Guioa,Lophostemon,Banksia and Helianthus honeys and their potential for floral authentication.Food Research International,2005,38(6):651-658.
[28]Penuelas J,Castells E,Joffre R,Tognetti R.Carbon-based secondary and structural compounds in Mediterranean shrubs growing near a natural CO 2 spring.Global Change Biology,2002,8(3):281-288.
[29]Rossi A M,Stiling P,Moon D C,Cattell M V,Drake B G.Induced defensive response of myrtle oak to foliar insect herbivory in ambient and elevated CO 2.Journal of Chemical Ecology,2004,30(6):1143-1152.
[30]Chen F J,Wu G,Ge F,Parajulee M N,Shrestha R B.Effects of elevated CO 2 and transgenic Bt cotton on plant chemistry,performance,and feeding of an insect herbivore,the cotton bollworm.Entomologia Experimentalis et Applicata,2005,115(2):341-350.
[31]Coley P D,Massa M,Lovelock C E,Winter K.Effects of elevated CO 2 on foliar chemistry of saplings of nine species of tropical tree.Oecologia,2002,133(1):62-69.
[32]Qin J D,Wang C Z.The relation of interaction between insects and plants to evolution.Acta Entomologica Sinica,2001,44(3):360-365.
[33]Potts S G,Vulliamy B,Dafni A,Ne'eman G,Willmer P.Linking bees and flowers:How do floral communities structure pollinator communitiesEcology,2003,84(10):2628-2642.
[34]Kleijn D,Raemakers I.A retrospective analysis of pollen host plant use by stable and declining bumble bee species.Ecology,2008,89(7):1811-1823.
[35]Liu F L,Zhang X W,Chai J P,Yang D R.Pollen phenolics and regulation of pollen foraging in honeybee colony.Behavioral Ecology and Sociobiology,2006,59(4):582-588.
[36]Kessler D,Gase K,Baldwin I T.Field experiments with transformed plants reveal the sense of floral scents.Science,2008,321(5893):1200-1202.
[37]Rhoades D F,Bergdahl J C.Adaptive significance of toxic nectar.The American Naturalist,1981,117(5):798-803.
[23]薛敬意,唐建维,沙丽清,孟盈.西双版纳望天树林土壤养分含量及其季节变化.植物生态学报,2003,27(3):373-379.
[26]兰国玉,胡跃华,曹敏,朱华,王洪,周仕顺,邓晓保,崔景云,黄建国,刘林云,许海龙,宋军平,何有才.西双版纳热带森林动态监测样地——树种组成与空间分布格局.植物生态学报,2008,32(2):287-298.
[32]钦俊德,王琛柱.论昆虫与植物的相互作用和进化的关系.昆虫学报,2001,44(3):360-365.