油用牡丹‘凤丹’主要传粉昆虫的传粉行为比较
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摘要
【目的】显花植物大多具有多种传粉者,判断最有效传粉者的直接证据是对主要传粉者的传粉效率进行研究。‘凤丹’(Paeonia ostii‘Feng Dan’)为一种新型木本食用油料植物,繁育系统为部分自交亲和、异交,需要传粉者活动才能完成授粉过程。笔者对‘凤丹’居群的访花昆虫种类及其传粉行为进行研究,旨在查清‘凤丹’主要传粉昆虫种类及其传粉效率,为提高‘凤丹’结籽率、改善种子质量、加大栽培规模提供传粉生物学参考。【方法】采用定点调查法对‘凤丹’主要传粉昆虫及其访花频率、单花停留时间、访花时柱头接触率进行观测,采用跟踪调查法对主要传粉昆虫连续两次访花的飞行距离、访固定花朵数目时的被访植株数进行观测,通过田间采集与室内镜检对主要传粉昆虫体表携粉量与单次访花后柱头花粉落置量进行统计。【结果】‘凤丹’访花昆虫主要有蜂类、蚁类、甲虫类及蝇类共4个类群,主要传粉昆虫为意大利蜜蜂(Apis mellifera)、中华蜜蜂(A.cerana)与黄熊蜂(Bombus flavescens)。意大利蜜蜂与中华蜜蜂的访花行为相似。黄熊蜂的访花频率极显著高于意大利蜜蜂和中华蜜蜂的(P<0.01),单花停留时间极显著低于意大利蜜蜂和中华蜜蜂的(P<0.01);黄熊蜂的柱头接触率与意大利蜜蜂及中华蜜蜂的差异不显著。黄熊蜂的访花飞行距离极显著高于意大利蜜蜂和中华蜜蜂的(P<0.01),访固定花朵数目时的被访植株数极显著高于意大利蜜蜂和中华蜜蜂的(P<0.01),更能促进植株的异交授粉。黄熊蜂的体表携粉量极显著高于意大利蜜蜂和中华蜜蜂的(P<0.01),单次访花后柱头花粉落置量极显著高于意大利蜜蜂和中华蜜蜂的(P<0.01),花粉转移能力更高。【结论】黄熊蜂、意大利蜜蜂和中华蜜蜂均为‘凤丹’有效传粉昆虫,以黄熊蜂传粉效率最高,中华蜜蜂与意大利蜜蜂其次,二者具有相近传粉效率。
【Objective】 Many Paeonia plants have poor fecundity. Paeonia ostii ‘Feng Dan'is a shrub that originated from Anhui Province and now planted widely in Hunan, Chongqing, Shandong, Sichuan and Henan in China. P. ostii seed contains abundant monounsaturated fatty acid, including α-linolenic acid(ALA), an essential fatty acid that humans cannot synthesize. Thus, the seed of P. ostii is an excellent raw material for the production of a new type of edible oil. Compared with the low fruit set of other Paeonia plants, the fruit set of P. ostii is high, which provides the possibility for large-scale production of its seed. The seed set of P. ostii from cross-pollination is significantly higher than that from self-pollination, which means that seed production is outcross pollinated and pollinator dependent. Thus, the foraging behavior of the main P. ostii pollinators is still unclear, which is important for gaining higher yield and seed quality. 【Method】 We investigated the pollination behavior of the major pollinators of P. ostii in Dianjing, Northeastern Chongqing, China in March and April from 2015 to 2017. Through fixed-point observations, we examined the visiting frequency, residence time, and rate of stigma contact of major pollinators. Through tracking observation, we measured the flying distance of main pollinators between two consecutive visits using a portable infrared rangefinder(Shendawei SW-A/B, Dongguan, China). Occasionally, honeybees flew away and returned to revisit the same flower, which was regarded as a single visit. Through field collections and laboratory observations under a microscope, we observed the pollen load of the main pollinators by netting the forager from the visited flower, and then transferring them to a poison flask and taking to the laboratory. All pollen grains on the poison flask and on the surface of the pollinator body were flushed with 50% alcohol and transferred onto a glass slide before being observed and counted under a microscope. The source of pollen grains was not identified; in our preliminary observation, all pollen grains carried by bees were found to be from P. ostii under a scanning electron microscope. To confirm pollen deposition by the main pollinators on the stigma after a single visit, the unopen flower was bagged until opening. The petals of the large flower were taped to form a half closure after fully opening, which allowed the pollinator to contact the stigma before collecting pollen grains. When the stigma was visited by a pollinator, it was transferred into a centrifuge tube and brought into the laboratory to observe and count under microscope. 【Result】 ①Visitors to P. ostii flowers included ants(Plagiolepis wroughtoni Forel, Pheidole rhombinoda Mayr., Crematogaster politula Forel, Paratrechina bourbonica Forel), beetles(Oxycetonia bealiae Gory et Percheron, Themus sp., Altica cyanea Weber, Basilepta sp.), flies(Lucilia cuprina Wied, Metallea notate Wulp) and bees(Apis mellifera, A. cerana, Bombus flavescens). The main pollinators of P. ostii flowers were Apis mellifera, A. cerana, and B. flavescens, due to their large numbers, speed when moving between different flowers, and the obvious pollen grains stuck to their body surface during visiting. ② Among three species of bees, both A. mellifera and A. cerana were similar in terms of pollinating behavior. Apis mellifera and A. cerana collected pollen grains from anthers with legs, while B. flavescens applied buzz foraging pollen during visiting. Compared to A. mellifera and A. cerana, B. flavescens had a shorter handle time(P<0.01) and a higher visiting frequency(P<0.01). Rates of stigma contact by all three bee species were low because of the relative spatial separation between anther and stigma in the large-sized flower after its opening. There was no significant difference in the rate of stigma contact among the three bee species(P=0.28), partly due to B. flavescens occasionally laying on the basal flower to collect pollen, which reduced its rate of stigma contact. ③ A. mellifera and A. cerana preferred to collect pollen grains from nearby flowers and plants. Bombus flavescens would continue its flight to reach distant flowers after foraging one-three flowers in the neighborhood. The flying distance of B. flavescens was significantly greater than that of A. mellifera and A. cerana(P<0.01). When visiting a fixed number of peony flowers, B. flavescens was distributed more widely(visiting more trees) than A. mellifera and A. cerana(P<0.01). ④ The surface of the pollen grain from P. ostii was dry, while that of its stigma was wet, and an obvious exudate could be observed on the stigma if it remained unpollinated on the third flowering day. During foraging, pollen grains could be stuck to the legs, abdomen, and proboscis of the three bee species, and to the back of B. flavescens. Pollen load and deposition after a single visit of B. flavescens were significantly higher than those of A. mellifera and A. cerana(P<0.01), indicating that the bumble bee had a greater ability to transfer pollen.【Conclusion】 Apis mellifera, A. cerana and B. flavescens were effective pollinators of P. ostii flowers. The most efficient pollinator was B. flavescens, followed by A. cerana and A. mellifera with similar pollination efficiency.
【Objective】 Many Paeonia plants have poor fecundity. Paeonia ostii ‘Feng Dan'is a shrub that originated from Anhui Province and now planted widely in Hunan, Chongqing, Shandong, Sichuan and Henan in China. P. ostii seed contains abundant monounsaturated fatty acid, including α-linolenic acid(ALA), an essential fatty acid that humans cannot synthesize. Thus, the seed of P. ostii is an excellent raw material for the production of a new type of edible oil. Compared with the low fruit set of other Paeonia plants, the fruit set of P. ostii is high, which provides the possibility for large-scale production of its seed. The seed set of P. ostii from cross-pollination is significantly higher than that from self-pollination, which means that seed production is outcross pollinated and pollinator dependent. Thus, the foraging behavior of the main P. ostii pollinators is still unclear, which is important for gaining higher yield and seed quality. 【Method】 We investigated the pollination behavior of the major pollinators of P. ostii in Dianjing, Northeastern Chongqing, China in March and April from 2015 to 2017. Through fixed-point observations, we examined the visiting frequency, residence time, and rate of stigma contact of major pollinators. Through tracking observation, we measured the flying distance of main pollinators between two consecutive visits using a portable infrared rangefinder(Shendawei SW-A/B, Dongguan, China). Occasionally, honeybees flew away and returned to revisit the same flower, which was regarded as a single visit. Through field collections and laboratory observations under a microscope, we observed the pollen load of the main pollinators by netting the forager from the visited flower, and then transferring them to a poison flask and taking to the laboratory. All pollen grains on the poison flask and on the surface of the pollinator body were flushed with 50% alcohol and transferred onto a glass slide before being observed and counted under a microscope. The source of pollen grains was not identified; in our preliminary observation, all pollen grains carried by bees were found to be from P. ostii under a scanning electron microscope. To confirm pollen deposition by the main pollinators on the stigma after a single visit, the unopen flower was bagged until opening. The petals of the large flower were taped to form a half closure after fully opening, which allowed the pollinator to contact the stigma before collecting pollen grains. When the stigma was visited by a pollinator, it was transferred into a centrifuge tube and brought into the laboratory to observe and count under microscope. 【Result】 ①Visitors to P. ostii flowers included ants(Plagiolepis wroughtoni Forel, Pheidole rhombinoda Mayr., Crematogaster politula Forel, Paratrechina bourbonica Forel), beetles(Oxycetonia bealiae Gory et Percheron, Themus sp., Altica cyanea Weber, Basilepta sp.), flies(Lucilia cuprina Wied, Metallea notate Wulp) and bees(Apis mellifera, A. cerana, Bombus flavescens). The main pollinators of P. ostii flowers were Apis mellifera, A. cerana, and B. flavescens, due to their large numbers, speed when moving between different flowers, and the obvious pollen grains stuck to their body surface during visiting. ② Among three species of bees, both A. mellifera and A. cerana were similar in terms of pollinating behavior. Apis mellifera and A. cerana collected pollen grains from anthers with legs, while B. flavescens applied buzz foraging pollen during visiting. Compared to A. mellifera and A. cerana, B. flavescens had a shorter handle time(P<0.01) and a higher visiting frequency(P<0.01). Rates of stigma contact by all three bee species were low because of the relative spatial separation between anther and stigma in the large-sized flower after its opening. There was no significant difference in the rate of stigma contact among the three bee species(P=0.28), partly due to B. flavescens occasionally laying on the basal flower to collect pollen, which reduced its rate of stigma contact. ③ A. mellifera and A. cerana preferred to collect pollen grains from nearby flowers and plants. Bombus flavescens would continue its flight to reach distant flowers after foraging one-three flowers in the neighborhood. The flying distance of B. flavescens was significantly greater than that of A. mellifera and A. cerana(P<0.01). When visiting a fixed number of peony flowers, B. flavescens was distributed more widely(visiting more trees) than A. mellifera and A. cerana(P<0.01). ④ The surface of the pollen grain from P. ostii was dry, while that of its stigma was wet, and an obvious exudate could be observed on the stigma if it remained unpollinated on the third flowering day. During foraging, pollen grains could be stuck to the legs, abdomen, and proboscis of the three bee species, and to the back of B. flavescens. Pollen load and deposition after a single visit of B. flavescens were significantly higher than those of A. mellifera and A. cerana(P<0.01), indicating that the bumble bee had a greater ability to transfer pollen.【Conclusion】 Apis mellifera, A. cerana and B. flavescens were effective pollinators of P. ostii flowers. The most efficient pollinator was B. flavescens, followed by A. cerana and A. mellifera with similar pollination efficiency.
引文
[1] HEGLAND S J,GRYTNES J A,TOTLAND ?.The relative importance of positive and negative interactions for pollinator attraction in a plant community[J].Ecological Research,2009,24(4):929-936.DOI:10.1007/s11284-008-0572-3.
[2] 罗长维,陈友.麻疯树花部特征及其对传粉昆虫的影响[J].南京林业大学学报(自然科学版),2017,41(1):55-60.DOI:10.3969/j.issn.1000-2006.2017.01.009.LUO C W,CHEN Y.Floral characteristics and its effect on insect pollination of Jatropha curcas L.[J].Journal of Nanjing Forestry University (Natural Sciences Edition),2017,41(1):55-60.
[3] 李俊兰,潘斌,格日勒,等.濒危植物柄扁桃的传粉者及其访花行为[J].生态学杂志,2011,30 (7):1370-1374.LI J L,PAN B,GE R L,et al.Pollination insects and their flower-visiting behaviors on endangered plant Amygdalus pedunculata[J].Chinese Journal of Ecology,2011,30 (7):1370-1374.
[4] WANG X Y,QUAN Q M,WANG B,et al.Pollen competition between morphs in a pollen-color dimorphic herb and the loss of phenotypic polymorphism within populations[J].Evolution,2018,72(4):785-797.DOI:10.1111/evo.13445.
[5] 杨汉波,张蕊,宋平,等.木荷主要传粉昆虫的传粉行为[J].生态学杂志,2017,36(5):1322-1329.DOI:10.13292/j.1000-4890.201705.027.YANG H B,ZHANG R,SONG P,et al.Pollination behaviors of main insect pollinators of Schima superba (Theaceae)[J].Chinese Journal of Ecology,2017,36 (5):1322-1329.
[6] FENSTER C B,ARMBRUSTER W S,WILSON P,et al.Pollination syndromes and floral specialization[J].Annual Review of Ecology,Evolution,and Systematics,2004,35(1):375-403.DOI:10.1146/annurev.ecolsys.34.011802.132347.
[7] WASER N.Specialization and generalization in plant-pollinator interactions:a historical perspective[M]//WASER N M,OLLERTON J.Plant-pollinator interactions:from specialization to generalization.Chicago:University of Chicago Press,2006:3-17.
[8] 张涛,高天姝,白瑞英,等.油料牡丹利用与研究进展[J].重庆师范大学学报(自然科学版),2015,32(2):138-144.ZHANG T,GAO T S,BAI R Y,et al.Utilization and research progress of oil tree peony [J].Journal of Chongqing Normal University (Natural Science),2015,32(2):138-144.
[9] 司冰.油料牡丹“凤丹”的授粉特性研究[D].杨凌:西北农林科技大学,2016:1-11.SI B.Chracteristics of pollination in Paeonia ostii ‘Feng Dan’ in the oil cultivation system[D].Yangling:Northwest A&F University,2016:1-11.
[10] XIE L H,NIU L X,ZHANG Y L,et al.Pollen sources influence the traits of seed and seed oil in Paeonia ostii ‘Feng Dan’[J].Hort Science,2017,52(5):700-705.DOI:10.21273/hortsci11803-17.
[11] TURPIN R A,SCHLISING R A.A new method for studying pollen dispersal using iodine[J].Radiation Botany,1971,11 (1):75-78.
[12] SCHLISING R A.Reproductive proficiency in Paeonia californica (Paeoniaceae) [J].American Journal of Botany,1976,63 (8):1095-1103.
[13] 罗毅波,裴颜龙,潘开玉,等.矮牡丹传粉生物学的初步研究[J].植物分类学报,1998,36(2):134-144.LUO Y B,PEI Y L,PAN K Y,et al.A study on pollination biology of Paeonia suffruticosa subsp.spontanea (Paeoniaceae) [J].Acta Phytotaxonomica Sinica,1998,36(2):134-144.
[14] 罗长维,陈友,张涛.凤丹繁育系统与传粉生物学研究[J].南京林业大学学报(自然科学版),2019,43(3):37-44.DOI:10.3969/j.issn.1000-2006.201808049.LUO C W,CHEN Y,ZHANG T.Breeding system and pollination biology of Paeonia ostii T.Hong & J.X.Zhang[J].Journal of Nanjing Forestry University (Natural Sciences Edition),2019,43(3):37-44.
[15] 罗长维,李昆,陈晓鸣,等.干热河谷麻疯树访花昆虫及主要传粉昆虫[J].昆虫知识,2008,45(1):121-127.LUO C W,LI K,CHEN X M,et al.Foraging and main pollinators of Jatropha curcas in dry-hot valley[J].Chinese Bulletin of Entomology,2008,45(1):121-127.
[16] 杨勇,骆劲涛,张必芳,等.四川牡丹的花部特征和繁育系统研究[J].植物资源与环境学报,2015,24(4):97-104.DOI:10.3969/j.issn.1674-7895.2015.04.13.YANG Y,LUO J T,ZHANG B F,et al.Studies on floral characteristics and breeding system of Paeonia decomposita[J].Journal of Plant Resources and Environment,2015,24(4):97-104.
[17] LI K,ZHENG B,WANG Y,et al.Breeding system and pollination biology of Paeonia delavayi (Paeoniaceae),an endangered plant in the southwest of China [J].Pakistan Journal of Botany,2014,46(5):1631-1642.
[18] 红雨,刘强.芍药的访花昆虫和传粉昆虫[J].昆虫知识,2004,41(5):449-454.HONG Y,LIU Q.Foraging and pollination insects of Paeonia lactiflom [J].Entomological Knowledge,2004,41(5):449-454.
[19] AMORIM F W,GALETTO L,SAZIMA M.Beyond the pollination syndrome:nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae) [J].Plant Biology,2013,15(2):317-327.DOI:10.1111/j.1438-8677.2012.00643.x.
[20] AGUILAR-RODRíGUEZ P A,KR?MER T,GARCíA‐FRANCO J G,et al.From dusk till dawn:nocturnal and diurnal pollination in the epiphyte Tillandsia heterophylla (Bromeliaceae)[J].Plant Biology,2016,18(1):37-45.DOI:10.1111/plb.12319.
[21] 胡红岩,陈欢,徐环李.毛乌素沙地固沙植物披针叶黄华主要传粉昆虫及其访花行为[J].生物多样性,2012,20(3):354-359.DOI:10.3724/SP.J.1003.2012.06240.HU H Y,CHEN H,XU H L.Main pollinators and their foraging behaviors on a sand-fixing legume,Thermopsis lanceolata,in Mu Us Sandland[J].Biodiversity,2012,20(3):354-359.
[22] THOMSON J D,GOODELL K.Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers[J].Journal of Applied Ecology,2002,38(5):1032-1044.DOI:10.1046/j.1365-2664.2001.00657.x.
[23] LUO C W,HUANG Z Y,CHEN X M,et al.Contribution of diurnal and nocturnal insects to the pollination of Jatropha curcas (Euphorbiaceae) in Southwestern China[J].Journal of Economic Entomology,2011,104(1):149-154.DOI:10.1603/EC10265.
[24] 周志勇,张红,梁铖,等.西方蜜蜂和兰州熊蜂在设施桃园的访花偏好性比较[J].昆虫学报,2015,58(12) :1315-1321.DOI:10.16380 /j.kcxb.2015.12.007ZHOU Z Y,ZHANG H,LIANG C,et al.Foraging preference of the honeybee Apis mellifera and the bumblebee Bombus lantschouensis (Hymenoptera:Apidae) in peach greenhouse[J].Acta Entomologica Sinica,2015,58(12) :1315-1321.
[25] GOULSON D,DARVILL B.Niche overlap and diet breadth in bumblebees:are rare species more specialized in their choice of flowers?[J].Apidologie,2004,35(1):55-63.DOI:10.1051/apido:2003062.
[26] FONTAINE C,COLLIN C L,DAJOZ I.Generalist foraging of pollinators:diet expansion at high density [J].Journal of Ecology,2008,96(5):1002-1010.DOI:10.1111/j.1365-2745.2008.01405.x.
[27] SOMME L,VANDERPLANCK M,MICHEZ D,et al.Pollen and nectar quality drive the major and minor floral choices of bumble bees[J].Apidologie,2015,46(1):92-106.DOI:10.1007/s13592-014-0307-0.
[28] MOQUET L,BRUYèRE L,PIRARD B,et al.Nectar foragers contribute to the pollination of buzz-pollinated plant species[J].Americal Journal of Botany,2017,104(10):1451-1463.DOI:10.3732/ajb.1700090.
[29] ADLER L S,IRWIN R E.Comparison of pollen transfer dynamics by multiple floral visitors:experiments with pollen and fluorescent dye[J].Annals of Botany,2006,97(1):141-150.DOI:10.1093/aob/mcj012.
[30] 李江红.影响蜜蜂为农作物授粉效能的因素分析[J].农学学报,2015,5 (9):104-109.LI J H.Analysis of the factors affecting honeybee pollination efficiency for agricultural crops[J].Journal of Agriculture,2015,5(9):104-109.
[31] 苏晓玲,华启云,陈伊凡,等.中华蜜蜂和意大利蜜蜂夏季高温下为长季节栽培设施西瓜授粉行为观察[J].环境昆虫学报,2017,39 (1):104-110.DOI:10.3969 /j.issn.1674-0858.2017.01.12.SU X L,HUA Q Y,CHEN Y F,et al.Behavior of Apis cerana cerana and Apis mellifera ligustica as pollinator for long-season cultivated watermelon in tunnel greenhouse under summer high temperature condition [J].Journal of Environmental Entomology,2017,39 (1):104-110.
[2] 罗长维,陈友.麻疯树花部特征及其对传粉昆虫的影响[J].南京林业大学学报(自然科学版),2017,41(1):55-60.DOI:10.3969/j.issn.1000-2006.2017.01.009.LUO C W,CHEN Y.Floral characteristics and its effect on insect pollination of Jatropha curcas L.[J].Journal of Nanjing Forestry University (Natural Sciences Edition),2017,41(1):55-60.
[3] 李俊兰,潘斌,格日勒,等.濒危植物柄扁桃的传粉者及其访花行为[J].生态学杂志,2011,30 (7):1370-1374.LI J L,PAN B,GE R L,et al.Pollination insects and their flower-visiting behaviors on endangered plant Amygdalus pedunculata[J].Chinese Journal of Ecology,2011,30 (7):1370-1374.
[4] WANG X Y,QUAN Q M,WANG B,et al.Pollen competition between morphs in a pollen-color dimorphic herb and the loss of phenotypic polymorphism within populations[J].Evolution,2018,72(4):785-797.DOI:10.1111/evo.13445.
[5] 杨汉波,张蕊,宋平,等.木荷主要传粉昆虫的传粉行为[J].生态学杂志,2017,36(5):1322-1329.DOI:10.13292/j.1000-4890.201705.027.YANG H B,ZHANG R,SONG P,et al.Pollination behaviors of main insect pollinators of Schima superba (Theaceae)[J].Chinese Journal of Ecology,2017,36 (5):1322-1329.
[6] FENSTER C B,ARMBRUSTER W S,WILSON P,et al.Pollination syndromes and floral specialization[J].Annual Review of Ecology,Evolution,and Systematics,2004,35(1):375-403.DOI:10.1146/annurev.ecolsys.34.011802.132347.
[7] WASER N.Specialization and generalization in plant-pollinator interactions:a historical perspective[M]//WASER N M,OLLERTON J.Plant-pollinator interactions:from specialization to generalization.Chicago:University of Chicago Press,2006:3-17.
[8] 张涛,高天姝,白瑞英,等.油料牡丹利用与研究进展[J].重庆师范大学学报(自然科学版),2015,32(2):138-144.ZHANG T,GAO T S,BAI R Y,et al.Utilization and research progress of oil tree peony [J].Journal of Chongqing Normal University (Natural Science),2015,32(2):138-144.
[9] 司冰.油料牡丹“凤丹”的授粉特性研究[D].杨凌:西北农林科技大学,2016:1-11.SI B.Chracteristics of pollination in Paeonia ostii ‘Feng Dan’ in the oil cultivation system[D].Yangling:Northwest A&F University,2016:1-11.
[10] XIE L H,NIU L X,ZHANG Y L,et al.Pollen sources influence the traits of seed and seed oil in Paeonia ostii ‘Feng Dan’[J].Hort Science,2017,52(5):700-705.DOI:10.21273/hortsci11803-17.
[11] TURPIN R A,SCHLISING R A.A new method for studying pollen dispersal using iodine[J].Radiation Botany,1971,11 (1):75-78.
[12] SCHLISING R A.Reproductive proficiency in Paeonia californica (Paeoniaceae) [J].American Journal of Botany,1976,63 (8):1095-1103.
[13] 罗毅波,裴颜龙,潘开玉,等.矮牡丹传粉生物学的初步研究[J].植物分类学报,1998,36(2):134-144.LUO Y B,PEI Y L,PAN K Y,et al.A study on pollination biology of Paeonia suffruticosa subsp.spontanea (Paeoniaceae) [J].Acta Phytotaxonomica Sinica,1998,36(2):134-144.
[14] 罗长维,陈友,张涛.凤丹繁育系统与传粉生物学研究[J].南京林业大学学报(自然科学版),2019,43(3):37-44.DOI:10.3969/j.issn.1000-2006.201808049.LUO C W,CHEN Y,ZHANG T.Breeding system and pollination biology of Paeonia ostii T.Hong & J.X.Zhang[J].Journal of Nanjing Forestry University (Natural Sciences Edition),2019,43(3):37-44.
[15] 罗长维,李昆,陈晓鸣,等.干热河谷麻疯树访花昆虫及主要传粉昆虫[J].昆虫知识,2008,45(1):121-127.LUO C W,LI K,CHEN X M,et al.Foraging and main pollinators of Jatropha curcas in dry-hot valley[J].Chinese Bulletin of Entomology,2008,45(1):121-127.
[16] 杨勇,骆劲涛,张必芳,等.四川牡丹的花部特征和繁育系统研究[J].植物资源与环境学报,2015,24(4):97-104.DOI:10.3969/j.issn.1674-7895.2015.04.13.YANG Y,LUO J T,ZHANG B F,et al.Studies on floral characteristics and breeding system of Paeonia decomposita[J].Journal of Plant Resources and Environment,2015,24(4):97-104.
[17] LI K,ZHENG B,WANG Y,et al.Breeding system and pollination biology of Paeonia delavayi (Paeoniaceae),an endangered plant in the southwest of China [J].Pakistan Journal of Botany,2014,46(5):1631-1642.
[18] 红雨,刘强.芍药的访花昆虫和传粉昆虫[J].昆虫知识,2004,41(5):449-454.HONG Y,LIU Q.Foraging and pollination insects of Paeonia lactiflom [J].Entomological Knowledge,2004,41(5):449-454.
[19] AMORIM F W,GALETTO L,SAZIMA M.Beyond the pollination syndrome:nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae) [J].Plant Biology,2013,15(2):317-327.DOI:10.1111/j.1438-8677.2012.00643.x.
[20] AGUILAR-RODRíGUEZ P A,KR?MER T,GARCíA‐FRANCO J G,et al.From dusk till dawn:nocturnal and diurnal pollination in the epiphyte Tillandsia heterophylla (Bromeliaceae)[J].Plant Biology,2016,18(1):37-45.DOI:10.1111/plb.12319.
[21] 胡红岩,陈欢,徐环李.毛乌素沙地固沙植物披针叶黄华主要传粉昆虫及其访花行为[J].生物多样性,2012,20(3):354-359.DOI:10.3724/SP.J.1003.2012.06240.HU H Y,CHEN H,XU H L.Main pollinators and their foraging behaviors on a sand-fixing legume,Thermopsis lanceolata,in Mu Us Sandland[J].Biodiversity,2012,20(3):354-359.
[22] THOMSON J D,GOODELL K.Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers[J].Journal of Applied Ecology,2002,38(5):1032-1044.DOI:10.1046/j.1365-2664.2001.00657.x.
[23] LUO C W,HUANG Z Y,CHEN X M,et al.Contribution of diurnal and nocturnal insects to the pollination of Jatropha curcas (Euphorbiaceae) in Southwestern China[J].Journal of Economic Entomology,2011,104(1):149-154.DOI:10.1603/EC10265.
[24] 周志勇,张红,梁铖,等.西方蜜蜂和兰州熊蜂在设施桃园的访花偏好性比较[J].昆虫学报,2015,58(12) :1315-1321.DOI:10.16380 /j.kcxb.2015.12.007ZHOU Z Y,ZHANG H,LIANG C,et al.Foraging preference of the honeybee Apis mellifera and the bumblebee Bombus lantschouensis (Hymenoptera:Apidae) in peach greenhouse[J].Acta Entomologica Sinica,2015,58(12) :1315-1321.
[25] GOULSON D,DARVILL B.Niche overlap and diet breadth in bumblebees:are rare species more specialized in their choice of flowers?[J].Apidologie,2004,35(1):55-63.DOI:10.1051/apido:2003062.
[26] FONTAINE C,COLLIN C L,DAJOZ I.Generalist foraging of pollinators:diet expansion at high density [J].Journal of Ecology,2008,96(5):1002-1010.DOI:10.1111/j.1365-2745.2008.01405.x.
[27] SOMME L,VANDERPLANCK M,MICHEZ D,et al.Pollen and nectar quality drive the major and minor floral choices of bumble bees[J].Apidologie,2015,46(1):92-106.DOI:10.1007/s13592-014-0307-0.
[28] MOQUET L,BRUYèRE L,PIRARD B,et al.Nectar foragers contribute to the pollination of buzz-pollinated plant species[J].Americal Journal of Botany,2017,104(10):1451-1463.DOI:10.3732/ajb.1700090.
[29] ADLER L S,IRWIN R E.Comparison of pollen transfer dynamics by multiple floral visitors:experiments with pollen and fluorescent dye[J].Annals of Botany,2006,97(1):141-150.DOI:10.1093/aob/mcj012.
[30] 李江红.影响蜜蜂为农作物授粉效能的因素分析[J].农学学报,2015,5 (9):104-109.LI J H.Analysis of the factors affecting honeybee pollination efficiency for agricultural crops[J].Journal of Agriculture,2015,5(9):104-109.
[31] 苏晓玲,华启云,陈伊凡,等.中华蜜蜂和意大利蜜蜂夏季高温下为长季节栽培设施西瓜授粉行为观察[J].环境昆虫学报,2017,39 (1):104-110.DOI:10.3969 /j.issn.1674-0858.2017.01.12.SU X L,HUA Q Y,CHEN Y F,et al.Behavior of Apis cerana cerana and Apis mellifera ligustica as pollinator for long-season cultivated watermelon in tunnel greenhouse under summer high temperature condition [J].Journal of Environmental Entomology,2017,39 (1):104-110.
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