两种象甲幼虫肠道微生物组成及对高单宁食物的适应
|
摘要
【目的】象甲是栎属植物橡子中主要的寄生昆虫,但其适应高单宁食物(橡子)的肠道微生物基础尚待揭示。本研究分析了蒙古栎和辽东栎橡子中两种柞栎象(Curculio arakawai和C.dentipes)幼虫的肠道菌群结构和多样性,试图阐明柞栎象幼虫适应高单宁食物的肠道微生物基础。【方法】分别提取蒙古栎和辽东栎橡子中象甲幼虫各50头的肠道DNA,利用Illumina MiSeq技术对肠道菌群的V3–V4区序列进行16S rRNA测序,统计样品操作分类单元(OTU)数量,分析物种组成丰度、α多样性和β多样性。【结果】结果表明,可用于物种分类的OTU分别有2054和2308个,C. arakawai和C. dentipes共有的OUT 481个。在两种柞栎象C. arakawai和C. dentipes肠道菌群中,共注释到的主要分类阶元有27个门、145个科和274个属。变形菌门(Proteobacteria)、拟杆菌门(Bacteroidetes)和厚壁菌门(Firmicutes)在两种象甲肠道菌群中占优势;假单胞菌属Pseudomonas(63.8%)、沙雷氏菌属Serratia(6%)和不动杆菌属Acinetobacter (5.2%)是C. arakawai肠道中的主要类群,而沙雷氏菌属Serratia (32%)、拉恩菌属Rahnella(24.2%)、气单胞菌属Aeromonas(6.8%)和立克次体属Rickettsia(6.6%)在C.dentipes肠道菌群中占主导优势。C. arakawai和C. dentipes肠道菌群α多样性无显著差异,β多样性则差异显著。具有单宁酶活性的肠道细菌,如粘质沙雷菌Serratia marcescens、乳球菌Lactococcus lactis、假单胞菌Pseudomonas spp.在C. arakawai和C. dentipes之间差异不显著。【结论】寄生在蒙古栎和辽东栎橡子中的C. arakawai和C.dentipes肠道菌群组成迥异,这可能与遗传因素和食物特点有关。具有单宁酶活性的粘质沙雷氏菌Serratia marcescens和乳球菌Lactococcus lactis等菌类可能是两种象甲幼虫适应高单宁食物的肠道微生物基础。
[Objective] Curculio beetles are major parasitic insects of oak acorns, but the mechanism of their adaptation to high-tannin food(e.g., acorns) is not clear. In this study, we compared the structure and diversity of gut bacteria of the larvae of Curculio arakawai and C. dentipes infested in Mongolian oak(Quercus mongolica) and Liaodong oak(Q. liaotungensis), to elucidate the adaptive mechanisms of weevil larvae to high-tannin food.[Methods] We collected gut samples of weevil larvae for DNA extraction. V3–V4 areas were sequenced using the Illumina MiSeq technology 16S rRNA sequencing. We carried out sequence statistics of Operational Taxonomic Units(OTUs), analysis of species abundance, a and b diversity. [Results] There were 2054 OTUs and 2308 OTUs of the high quality sequences obtained from the guts of the 2 weevil species, in which 481 OTUs were shared. In the gut bacterial community of C. arakawai and C. dentipes, 27 phyla, 145 families and 274 genera were identified as the major taxonomic groups. At the phylum level, Proteobacteria, Bacteroidetes and Firmicutes were dominant in the guts of C. arakawai and C. dentipes. At the genus level, Pseudomonas(63.8%), Serratia(6%) and Acinetobacter(5.2%) were the main groups in the gut of C. arakawai, while Serratia(32%), Rahnella(24.2%),Aeromonas(6.8%) and Rickettsia(6.6%) were dormant in the gut of C. dentipes. Our a diversity analyses showed no significant differences between the gut bacteria of C. arakawai and C. dentipes; however, b diversity showed significant difference between the gut bacteria of C. arakawai and C. dentipes. [Conclusion] Differences in gut bacterial community may be related to differences in species of weevils and host tannin content. We also found several bacteria related to the degradation of tannins, e.g., Serratia marcescens and Lactococcus lactis, which may reflect the adaptive basis for two weevil species to use high tannin food.
[Objective] Curculio beetles are major parasitic insects of oak acorns, but the mechanism of their adaptation to high-tannin food(e.g., acorns) is not clear. In this study, we compared the structure and diversity of gut bacteria of the larvae of Curculio arakawai and C. dentipes infested in Mongolian oak(Quercus mongolica) and Liaodong oak(Q. liaotungensis), to elucidate the adaptive mechanisms of weevil larvae to high-tannin food.[Methods] We collected gut samples of weevil larvae for DNA extraction. V3–V4 areas were sequenced using the Illumina MiSeq technology 16S rRNA sequencing. We carried out sequence statistics of Operational Taxonomic Units(OTUs), analysis of species abundance, a and b diversity. [Results] There were 2054 OTUs and 2308 OTUs of the high quality sequences obtained from the guts of the 2 weevil species, in which 481 OTUs were shared. In the gut bacterial community of C. arakawai and C. dentipes, 27 phyla, 145 families and 274 genera were identified as the major taxonomic groups. At the phylum level, Proteobacteria, Bacteroidetes and Firmicutes were dominant in the guts of C. arakawai and C. dentipes. At the genus level, Pseudomonas(63.8%), Serratia(6%) and Acinetobacter(5.2%) were the main groups in the gut of C. arakawai, while Serratia(32%), Rahnella(24.2%),Aeromonas(6.8%) and Rickettsia(6.6%) were dormant in the gut of C. dentipes. Our a diversity analyses showed no significant differences between the gut bacteria of C. arakawai and C. dentipes; however, b diversity showed significant difference between the gut bacteria of C. arakawai and C. dentipes. [Conclusion] Differences in gut bacterial community may be related to differences in species of weevils and host tannin content. We also found several bacteria related to the degradation of tannins, e.g., Serratia marcescens and Lactococcus lactis, which may reflect the adaptive basis for two weevil species to use high tannin food.
引文
[1]Fu LG,Chen TQ,Lang KY,Hong T,Lin Q,Li Y.Higher Plants in China(Vol.1).Qingdao:Qingdao Publishers,2012.(in Chinese)傅立国,陈潭清,郎楷永,洪涛,林祁,李勇.中国高等植物(第一卷).青岛:青岛出版社,2012.
[2]Li WY,Gu WC.Study on phenotypic diversity of natural population in Quercus mongolica.Scientia Silvae Sinicae,2005,41(1):49-56.(in Chinese)李文英,顾万春.蒙古栎天然群体表型多样性研究.林业科学,2005,41(1):49-56.
[3]Berasategui A,Axelsson K,Nordlander G,Schmidt A,Borg-Karlson AK,Gershenzon J,Terenius O,Kaltenpoth M.The gut microbiota of the pine weevil is similar across Europe and resembles that of other conifer-feeding beetles.Molecular Ecology,2016,25(16):4014-4031.
[4]Berasategui A,Salem H,Paetz C,Santoro M,Gershenzon J,Kaltenpoth M,Schmidt A.Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness.Molecular Ecology,2017,26(15):4099-4110.
[5]Morales-Jiménez J,Zú?iga G,Villa-Tanaca L,Hernández-Rodríguez C.Bacterial community and nitrogen fixation in the red turpentine beetle,Dendroctonus valens LeConte(Coleoptera:Curculionidae:Scolytinae).Microbial Ecology,2009,58(4):879-891.
[6]Rinke R,Costa AS,Fonseca FPP,Almeida LC,Delalibera I,Henrique-Silva F.Microbial diversity in the larval gut of field and laboratory populations of the sugarcane weevil Sphenophorus levis(Coleoptera,Curculionidae).Genetics and Molecular Research,2011,10(4):2679-2691.
[7]Xu LT,Lou QZ,Cheng CH,Lu M,Sun JH.Gut-associated bacteria of Dendroctonus valens and their involvement in verbenone production.Microbial Ecology,2015,70(4):1012-1023.
[8]Xu LT,Lu M,Xu DD,Chen L,Sun JH.Sexual variation of bacterial microbiota of Dendroctonus valens guts and frass in relation to verbenone production.Journal of Insect Physiology,2016,95:110-117.
[9]Xu LT,Shi ZH,Wang B,Lu M,Sun JH.Pine defensive monoterpeneα-pinene influences the feeding behavior of Dendroctonus valens and its gut bacterial community structure.International Journal of Molecular Sciences,2016,17(11):1734.
[10]Sun SC,Chen LZ.Seed demography of Quercus liaotungensis in Dongling mountain region.Acta Phytoecologica Sinica,2000,24(2):215-221.(in Chinese)孙书存,陈灵芝.东灵山地区辽东栎种子库统计.植物生态学报,2000,24(2):215-221.
[11]Wang X,Xiao ZS,Zhang ZB,Pan HC.Insect seed predation and its relationships with seed crop and seed size of Quercus mongolica.Acta Theriologica Sinica,2008,51(2):161-165.(in Chinese)王学,肖治术,张知彬,潘红春.昆虫种子捕食与蒙古栎种子产量和种子大小的关系.昆虫学报,2008,51(2):161-165.
[12]Yu XD,Zhou HZ,Luo TH.Spatial and temporal variations in insect-infested acorn fall in a Quercus liaotungensis forest in north China.Ecological Research,2003,18(2):155-164.
[13]Yu XD,Zhou HZ,Luo TH,He JJ,Zhang ZB.Insect infestation and acorn fate in Quercus liaotungensis.Acta Entomologica Sinica,2001,44(4):518-524.(in Chinese)于晓东,周红章,罗天宏,何君舰,张知彬.昆虫寄生对辽东栎种子命运的影响.昆虫学报,2001,44(4):518-524.
[14]Merville A,Venner S,Henri H,Vallier A,Menu F,Vavre F,Heddi A,Bel-Venner MC.Endosymbiont diversity among sibling weevil species competing for the same resource.BMC Evolutionary Biology,2013,13:28.
[15]Toju H,Hosokawa T,Koga R,Nikoh N,Meng XY,Kimura N,Fukatsu T.“Candidatus Curculioniphilus buchneri,”a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio.Applied and Environmental Microbiology,2010,76(1):275-282.
[16]Toju H,Tanabe AS,Notsu Y,Sota T,Fukatsu T.Diversification of endosymbiosis:Replacements,co-speciation and promiscuity of bacteriocyte symbionts in weevils.ISME Journal,2013,7(7):1378-1390.
[17]Toju H,Fukatsu T.Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil:Relevance of local climate and host plants.Molecular Ecology,2011,20(4):853-868.
[18]Berge O,Heulin T,Achouak W,Richard C,Bally R,Balandreau J.Rahnella aquatilis,a nitrogen-fixing enteric bacterium associated with the rhizosphere of wheat and maize.Canadian Journal of Microbiology,1991,37(3):195-203.
[19]Brady C,Denman S,Kirk S,Venter S,Rodríguez-Palenzuela P,Coutinho T.Description of Gibbsiella quercinecans gen.nov.,sp.nov.,associated with acute oak decline.Systematic and Applied Microbiology,2010,33(8):444-450.
[20]Bull CT,de Boer SH,Denny TP,Firrao G,Fischer-Le Saux M,Saddler GS,Scortichini M,Stead DE,Takikawa Y.List of new names of plant pathogenic bacteria(2008-2010).Journal of Plant Pathology,2012,94:21-27.
[21]Varsha,Mukherjee A,Bhanwar S,Ganguli A.Characterization of tannase production by Lactococcus lactis subsp.lactis and its potential in enhancing nutritional value of a composite sourdough.International Journal of Genetic Engineering and Biotechnology,2014,5(1):77-84.
[22]Belur PD,Mugeraya G.Microbial production of tannase:State of the art.Research Journal of Microbiology,2011,6(1):25-40.
[23]Selwal MK,Yadav A,Selwal KK,Aggarwal NK,Gupta R,Gautam SK.Optimization of cultural conditions for tannase production by Pseudomonas aeruginosa IIIB 8914 under submerged fermentation.World Journal of Microbiology and Biotechnology,2010,26(4):599-605.
[24]Osawa R,Mitsuoka T.Selective medium for enumeration of tannin-protein complex-degrading Streptococcus spp.in feces of koalas.Applied and Environmental Microbiology,1990,56(11):3609-3611.
[25]Sharma KP,John PJ.Purification and characterization of tannase and tannase gene from Enterobacter sp..Process Biochemistry,2011,46(1):240-244.
[26]Noguchi N,Ohashi T,Shiratori T,Narui K,Hagiwara T,Ko M,Watanabe K,Miyahara T,Taira S,Moriyasu F,Sasatsu M.Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene.Journal of Gastroenterology,2007,42(5):346-351.
[27]Pepi M,Lampariello LR,Altieri R,Esposito A,Perra G,Renzi M,Lobianco A,Feola A,Gasperini S,Focardi SE.Tannic acid degradation by bacterial strains Serratia spp.and Pantoea sp.isolated from olive mill waste mixtures.International Biodeterioration and Biodegradation,2010,64(1):73-80.
[28]Sasaki E,Shimada T,Osawa R,Nishitani Y,Spring S,Lang E.Isolation of tannin-degrading bacteria isolated from feces of the Japanese large wood mouse,Apodemus speciosus,feeding on tannin-rich acorns.Systematic and Applied Microbiology,2005,28(4):358-365.
[29]Osawa R,Fujisawa T,Pukall R.Lactobacillus apodemi sp.nov.,a tannase-producing species isolated from wild mouse faeces.International Journal of Systematic&Evolutionary Microbiology,2006,56:1693-1696.
[30]Kohl KD,Weiss RB,Dale C,Dearing MD.Diversity and novelty of the gut microbial community of an herbivorous rodent(Neotoma bryanti).Symbiosis,2011,54(1):47-54.
[31]Kohl KD,Dearing MD.Experience matters:Prior exposure to plant toxins enhances diversity of gut microbes in herbivores.Ecology Letters,2012,15(9):1008-1015.
[32]Osawa R,Kuroiso K,Goto S,Shimizu A.Isolation of tannin-degrading Lactobacilli from humans and fermented foods.Applied and Environmental Microbiology,2000,66(7):3093-3097.
[33]Shimada T,Saitoh T,Sasaki E,Nishitani Y,Osawa R.Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins.Journal of Chemical Ecology,2006,32(6):1165-1180.
[34]Steele MA,Hadj-Chikh LZ,Hazeltine J.Caching and feeding decisions by Sciurus carolinensis:Responses to weevil-infested acorns.Journal of Mammalogy,1996,77(2):305-314.
[35]Roehrig NE,Capinera JL.Behavioural and developmental responses of range caterpillar larvae,Hemileuca oliviae,to condensed tannin.Journal of Insect Physiology,1983,29(12):901-906.
[36]Zhu J,Filippich LJ,Alsalami MT.Tannic acid intoxication in sheep and mice.Research in Veterinary Science,1992,53(3):280-292.
[37]Johnson WC,Thomas L,Adkisson CS.Dietary circumvention of acorn tannins by blue jays-Implications for oak demography.Oecologia,1993,94(2):159-164.
[38]Shimada T,Nishii E,Saitoh T.Interspecific differences in tannin intakes of forest-dwelling rodents in the wild revealed by a new method using fecal proline content.Journal of Chemical Ecology,2011,37(12):1277-1284.
[39]Onodera R,Akimoto Y,Shimada T,Saitoh T.Different population responses of three sympatric rodent species to acorn masting-the role of tannin tolerance.Population Ecology,2017,59(1):29-43.
[40]Zhang ZB,Wang ZY,Chang G,Yi XF,Lu JQ,Xiao ZS,Zhang HM,Cao L,Wang FS,Li HJ,Yan C.Trade-off between seed defensive traits and impacts on interaction patterns between seeds and rodents in forest ecosystems.Plant Ecology,2016,217(3):253-265.
[2]Li WY,Gu WC.Study on phenotypic diversity of natural population in Quercus mongolica.Scientia Silvae Sinicae,2005,41(1):49-56.(in Chinese)李文英,顾万春.蒙古栎天然群体表型多样性研究.林业科学,2005,41(1):49-56.
[3]Berasategui A,Axelsson K,Nordlander G,Schmidt A,Borg-Karlson AK,Gershenzon J,Terenius O,Kaltenpoth M.The gut microbiota of the pine weevil is similar across Europe and resembles that of other conifer-feeding beetles.Molecular Ecology,2016,25(16):4014-4031.
[4]Berasategui A,Salem H,Paetz C,Santoro M,Gershenzon J,Kaltenpoth M,Schmidt A.Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness.Molecular Ecology,2017,26(15):4099-4110.
[5]Morales-Jiménez J,Zú?iga G,Villa-Tanaca L,Hernández-Rodríguez C.Bacterial community and nitrogen fixation in the red turpentine beetle,Dendroctonus valens LeConte(Coleoptera:Curculionidae:Scolytinae).Microbial Ecology,2009,58(4):879-891.
[6]Rinke R,Costa AS,Fonseca FPP,Almeida LC,Delalibera I,Henrique-Silva F.Microbial diversity in the larval gut of field and laboratory populations of the sugarcane weevil Sphenophorus levis(Coleoptera,Curculionidae).Genetics and Molecular Research,2011,10(4):2679-2691.
[7]Xu LT,Lou QZ,Cheng CH,Lu M,Sun JH.Gut-associated bacteria of Dendroctonus valens and their involvement in verbenone production.Microbial Ecology,2015,70(4):1012-1023.
[8]Xu LT,Lu M,Xu DD,Chen L,Sun JH.Sexual variation of bacterial microbiota of Dendroctonus valens guts and frass in relation to verbenone production.Journal of Insect Physiology,2016,95:110-117.
[9]Xu LT,Shi ZH,Wang B,Lu M,Sun JH.Pine defensive monoterpeneα-pinene influences the feeding behavior of Dendroctonus valens and its gut bacterial community structure.International Journal of Molecular Sciences,2016,17(11):1734.
[10]Sun SC,Chen LZ.Seed demography of Quercus liaotungensis in Dongling mountain region.Acta Phytoecologica Sinica,2000,24(2):215-221.(in Chinese)孙书存,陈灵芝.东灵山地区辽东栎种子库统计.植物生态学报,2000,24(2):215-221.
[11]Wang X,Xiao ZS,Zhang ZB,Pan HC.Insect seed predation and its relationships with seed crop and seed size of Quercus mongolica.Acta Theriologica Sinica,2008,51(2):161-165.(in Chinese)王学,肖治术,张知彬,潘红春.昆虫种子捕食与蒙古栎种子产量和种子大小的关系.昆虫学报,2008,51(2):161-165.
[12]Yu XD,Zhou HZ,Luo TH.Spatial and temporal variations in insect-infested acorn fall in a Quercus liaotungensis forest in north China.Ecological Research,2003,18(2):155-164.
[13]Yu XD,Zhou HZ,Luo TH,He JJ,Zhang ZB.Insect infestation and acorn fate in Quercus liaotungensis.Acta Entomologica Sinica,2001,44(4):518-524.(in Chinese)于晓东,周红章,罗天宏,何君舰,张知彬.昆虫寄生对辽东栎种子命运的影响.昆虫学报,2001,44(4):518-524.
[14]Merville A,Venner S,Henri H,Vallier A,Menu F,Vavre F,Heddi A,Bel-Venner MC.Endosymbiont diversity among sibling weevil species competing for the same resource.BMC Evolutionary Biology,2013,13:28.
[15]Toju H,Hosokawa T,Koga R,Nikoh N,Meng XY,Kimura N,Fukatsu T.“Candidatus Curculioniphilus buchneri,”a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio.Applied and Environmental Microbiology,2010,76(1):275-282.
[16]Toju H,Tanabe AS,Notsu Y,Sota T,Fukatsu T.Diversification of endosymbiosis:Replacements,co-speciation and promiscuity of bacteriocyte symbionts in weevils.ISME Journal,2013,7(7):1378-1390.
[17]Toju H,Fukatsu T.Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil:Relevance of local climate and host plants.Molecular Ecology,2011,20(4):853-868.
[18]Berge O,Heulin T,Achouak W,Richard C,Bally R,Balandreau J.Rahnella aquatilis,a nitrogen-fixing enteric bacterium associated with the rhizosphere of wheat and maize.Canadian Journal of Microbiology,1991,37(3):195-203.
[19]Brady C,Denman S,Kirk S,Venter S,Rodríguez-Palenzuela P,Coutinho T.Description of Gibbsiella quercinecans gen.nov.,sp.nov.,associated with acute oak decline.Systematic and Applied Microbiology,2010,33(8):444-450.
[20]Bull CT,de Boer SH,Denny TP,Firrao G,Fischer-Le Saux M,Saddler GS,Scortichini M,Stead DE,Takikawa Y.List of new names of plant pathogenic bacteria(2008-2010).Journal of Plant Pathology,2012,94:21-27.
[21]Varsha,Mukherjee A,Bhanwar S,Ganguli A.Characterization of tannase production by Lactococcus lactis subsp.lactis and its potential in enhancing nutritional value of a composite sourdough.International Journal of Genetic Engineering and Biotechnology,2014,5(1):77-84.
[22]Belur PD,Mugeraya G.Microbial production of tannase:State of the art.Research Journal of Microbiology,2011,6(1):25-40.
[23]Selwal MK,Yadav A,Selwal KK,Aggarwal NK,Gupta R,Gautam SK.Optimization of cultural conditions for tannase production by Pseudomonas aeruginosa IIIB 8914 under submerged fermentation.World Journal of Microbiology and Biotechnology,2010,26(4):599-605.
[24]Osawa R,Mitsuoka T.Selective medium for enumeration of tannin-protein complex-degrading Streptococcus spp.in feces of koalas.Applied and Environmental Microbiology,1990,56(11):3609-3611.
[25]Sharma KP,John PJ.Purification and characterization of tannase and tannase gene from Enterobacter sp..Process Biochemistry,2011,46(1):240-244.
[26]Noguchi N,Ohashi T,Shiratori T,Narui K,Hagiwara T,Ko M,Watanabe K,Miyahara T,Taira S,Moriyasu F,Sasatsu M.Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene.Journal of Gastroenterology,2007,42(5):346-351.
[27]Pepi M,Lampariello LR,Altieri R,Esposito A,Perra G,Renzi M,Lobianco A,Feola A,Gasperini S,Focardi SE.Tannic acid degradation by bacterial strains Serratia spp.and Pantoea sp.isolated from olive mill waste mixtures.International Biodeterioration and Biodegradation,2010,64(1):73-80.
[28]Sasaki E,Shimada T,Osawa R,Nishitani Y,Spring S,Lang E.Isolation of tannin-degrading bacteria isolated from feces of the Japanese large wood mouse,Apodemus speciosus,feeding on tannin-rich acorns.Systematic and Applied Microbiology,2005,28(4):358-365.
[29]Osawa R,Fujisawa T,Pukall R.Lactobacillus apodemi sp.nov.,a tannase-producing species isolated from wild mouse faeces.International Journal of Systematic&Evolutionary Microbiology,2006,56:1693-1696.
[30]Kohl KD,Weiss RB,Dale C,Dearing MD.Diversity and novelty of the gut microbial community of an herbivorous rodent(Neotoma bryanti).Symbiosis,2011,54(1):47-54.
[31]Kohl KD,Dearing MD.Experience matters:Prior exposure to plant toxins enhances diversity of gut microbes in herbivores.Ecology Letters,2012,15(9):1008-1015.
[32]Osawa R,Kuroiso K,Goto S,Shimizu A.Isolation of tannin-degrading Lactobacilli from humans and fermented foods.Applied and Environmental Microbiology,2000,66(7):3093-3097.
[33]Shimada T,Saitoh T,Sasaki E,Nishitani Y,Osawa R.Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins.Journal of Chemical Ecology,2006,32(6):1165-1180.
[34]Steele MA,Hadj-Chikh LZ,Hazeltine J.Caching and feeding decisions by Sciurus carolinensis:Responses to weevil-infested acorns.Journal of Mammalogy,1996,77(2):305-314.
[35]Roehrig NE,Capinera JL.Behavioural and developmental responses of range caterpillar larvae,Hemileuca oliviae,to condensed tannin.Journal of Insect Physiology,1983,29(12):901-906.
[36]Zhu J,Filippich LJ,Alsalami MT.Tannic acid intoxication in sheep and mice.Research in Veterinary Science,1992,53(3):280-292.
[37]Johnson WC,Thomas L,Adkisson CS.Dietary circumvention of acorn tannins by blue jays-Implications for oak demography.Oecologia,1993,94(2):159-164.
[38]Shimada T,Nishii E,Saitoh T.Interspecific differences in tannin intakes of forest-dwelling rodents in the wild revealed by a new method using fecal proline content.Journal of Chemical Ecology,2011,37(12):1277-1284.
[39]Onodera R,Akimoto Y,Shimada T,Saitoh T.Different population responses of three sympatric rodent species to acorn masting-the role of tannin tolerance.Population Ecology,2017,59(1):29-43.
[40]Zhang ZB,Wang ZY,Chang G,Yi XF,Lu JQ,Xiao ZS,Zhang HM,Cao L,Wang FS,Li HJ,Yan C.Trade-off between seed defensive traits and impacts on interaction patterns between seeds and rodents in forest ecosystems.Plant Ecology,2016,217(3):253-265.