引用本文
张丽, 袁明龙. 豌豆蚜生物生态学特性. 草业科学, 2017,34(8):1727-1740
Zhang Li, Yuan Ming-long. Biological and ecological characteristics of Acyrthosiphon pisum . Pratacultural Science,2017,34(8): 1727-1740  
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《草业科学》编辑部
豌豆蚜生物生态学特性
张丽1,2,3, 袁明龙1,2,3
1.草地农业生态系统国家重点实验室,兰州大学草地农业科技学院,甘肃 兰州 730020
2.草业科学国家级实验教学示范中心(兰州大学),甘肃 兰州 730020
3.农业部草牧业创新重点实验室,甘肃 兰州 730020
通信作者：袁明龙(1982-),男,甘肃靖远人,副教授,博士,主要从事草地昆虫学及分子生态学研究。E-mail:yuanml@lzu.edu.cn

第一作者:张丽(1993-),女,甘肃定西人,在读硕士生,主要从事草地昆虫学研究。E-mail:2516486351@qq.com

收稿日期: 2016-12-12
基金: 基金项目:甘肃省自然科学基金青年科技基金计划(1506RJZA211)
摘要

豌豆蚜( Acyrthosiphon pisum)是许多豆科作物及牧草的重要害虫,不但直接取食寄主植物,造成严重的经济损失,而且还会传播多种植物病毒。豌豆蚜作为生态学研究的模式昆虫,具有复杂的生活周期、多样的生殖方式、表型可塑性以及与细菌复杂的共生关系等诸多特点,已成为众多科学家感兴趣的研究对象。本文全面总结了豌豆蚜生物生态学特性的研究成果,重点综述了豌豆蚜的多型现象和内共生菌研究的最新进展,提出研究豌豆蚜在全球气候和作物种植结构变化下生物生态学特性演变规律的必要性,加强其生态适应性及多型现象等遗传机制研究,以期为建立该虫的可持续防控技术体系提供依据。

关键词: 蚜虫; 生物学特性; 表型可塑性; 孤雌生殖; 生态适应性
中图分类号:Q969.36+7.2 文献标志码:A 文章编号:1001-0629(2017)08-1727-14 doi: 10.11829/j.issn.1001-0629.2016-0518
Biological and ecological characteristics of Acyrthosiphon pisum
Zhang Li1,2,3, Yuan Ming-long1,2,3
1.State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
2.National Demonstration Center for Experimental Grassland Science Education (Lanzhou University) , Lanzhou 730020, China
3.Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture, Lanzhou University, Lanzhou 730020, China
Corresponding author: Yuan Ming-long E-mail:yuanml@lzu.edu.cn
Abstract

Acyrthosiphon pisum (Hemiptera, Aphidoidea, Aphididae) is an important insect pest of many crops and forage grasses. This pest not only causes serious losses to alfalfa production, but also is the vector of many plant viruses. As an ecological model insect, A. pisum fascinates many scientists due to its complex life cycle, multiple reproductive types, polymorphism and symbiotic relationship with bacteria. We summarized the research status of biological and ecological characteristics of A. pisum, especially for phenotypic polymorphisms and endosymbiotic bacteria. It is necessary to study how the biological characteristics of A. pisum respond to global climate and cropping pattern changes, and elucidate the genetic mechanisms of ecological adaptation and polymorphisms; this will be helpful for the establishment of sustainable management strategies for this pest.

Keyword: aphid; biological characteristics; phenotypic plasticity; parthenogernesis; ecological adaptation

中图分类号:Q969.36+7.2 文献标志码:A 文章编号:1001-0629(2017)08-1727-14

蚜虫是半翅目昆虫中较大的一个类群, 目前全世界已记录4 700余种, 其中我国约有1 000种, 主要分布在北半球温带地区和亚热带地区[1, 2, 3, 4]。许多蚜虫是重要的农林牧业害虫, 如麦长管蚜(Macrosiphum avenae)[5]、棉蚜(Aphis gossypii)[6-7]、桃蚜(Myzus persicae)[8]和豌豆蚜(Acyrthosiphon pisum)[9, 10, 11, 12]等。蚜虫以刺吸式口器吸食植物韧皮部汁液, 使植物营养损失, 发育受阻, 并出现畸形生长、早衰, 甚至死亡的现象[13, 14]; 同时, 许多蚜虫还是一些重要植物病毒的传播媒介[15]。此外, 蚜虫具有复杂的生活史和生殖方式[16], 高度表型可塑性[11, 12, 17], 这些特点使其成为众多昆虫学家、生态学家和进化生物学家最为感兴趣的研究对象之一[2, 9, 11, 18]。

豌豆蚜又称豆蚜、豆无网长管蚜, 属于蚜总科的蚜科(Aphididae), 该虫在世界各地广泛分布, 是许多豆科作物及牧草的主要害虫之一[19]。在美国, 豌豆蚜的危害可导致苜蓿生产者每年损失大约6 000万美元[20, 21]。在我国西北苜蓿种植区, 豌豆蚜每年可造成苜蓿生产10%~30%的经济损失[13, 22]。豌豆蚜危害植物时, 其若虫和成虫群集在植物的幼嫩部位, 以刺吸式口器吸取植物韧皮部汁液, 从而影响植物的生长发育、开花结实等正常的生命活动, 严重危害时甚至造成整块田间植株死亡[14, 23]。此外, 豌豆蚜还是苜蓿(Medicago sativa)花叶病毒、豌豆(Pisum sativum)耳突花叶病毒等25种病毒的主要传播者[15, 24, 25, 26]。由于豌豆蚜具有生活周期复杂、生殖方式多样、表型可塑性以及与细菌复杂的共生关系[12, 16, 17, 27, 28]等特点, 使其成为国际蚜虫基因组联盟科学家青睐的研究对象。2010年科学家采用鸟枪法成功完成了豌豆蚜全基因组序列的测定工作, 使其成为首个被破译基因组的蚜虫, 也是第一个被测序的半翅目昆虫[29]。近年来, 豌豆蚜的相关研究已逐渐深入到了组学水平, 使其成为遗传学、生态学及进化生物学研究的模式物种[17, 30, 31, 32, 33]。

豌豆蚜在我国各地均有发生, 且作为模式昆虫具有重要的研究价值, 明确豌豆蚜的生活史、发生规律、危害性及生态适应性等基础生物生态学特性, 是有效开展其预测预报及防治的前提和基础性工作。为此, 本文系统总结豌豆蚜生物生态学的研究现状, 深入分析已有研究成果, 并重点讨论今后应开展的研究方向, 以期为豌豆蚜的深入研究及有效防控提供理论支持。

1 生物学特性
1.1 世代及年生活史

豌豆蚜属于渐变态类昆虫, 包括卵、若虫和成虫3个发育阶段。该虫一年能繁殖十多代, 世代重叠现象严重[16]。豌豆蚜的发育历期在不同地区、不同气候条件下差异较大, 一般随温度的升高而缩短[16, 22]。田间条件下, 平均气温在12 ℃以上持续5 d时, 豌豆蚜便可开始繁殖[34]; 而在温室栽培的条件下, 全年均可繁殖危害[35]。但不论一年发生几代, 均以卵的形式越冬。豌豆蚜通常产卵于植物根部, 卵一般都单个分布, 数量多时也成群成堆。卵大多呈长椭圆形, 初生时为黄色, 然后逐渐变为绿色, 最后成为光亮黑色[16]。豌豆蚜在北方地区一般11月份产生两性蚜, 交尾后产卵于多年生豆科植物上越冬(图1), 而温暖地区或温室内全年不产生两性蚜[34, 36]。确定豌豆蚜的越冬场所并调查越冬卵基数, 有利于预测来年豌豆蚜的发生数量并指导有效防控。

图1 豌豆蚜生活史Fig. 1 Life cycle of the pea aphid

1.2 寄主及取食行为

豌豆蚜具有较为广泛的寄主植物, 不同的寄主植物对豌豆蚜的生长发育和繁殖均有影响。例如, 蚕豆(Vicia faba)和豌豆较红豆草(Onobrychis viciaefolia)更适合豌豆蚜的生长发育及繁殖[37, 38]。豌豆蚜取食蚕豆的不同品种, 其在发育历期、存活率以及生殖力方面均存在差异[38]。寄主植物不仅影响豌豆蚜的存活率和繁殖力, 而且会影响豌豆蚜的种群结构和遗传多样性[39]。同时寄主植物的干旱胁迫也能够影响豌豆蚜的习性和其在植物上的丰富度[40]。

豌豆蚜拥有强烈的寄主专化性[41, 42], 但这种特性因地而异。例如, 在纽约豌豆蚜寄主为苜蓿或红三叶草, 在加利福尼亚其寄主则主要为白三叶草(Trifolium repens), 我国分布的豌豆蚜则在苜蓿及豆科作物上取食[22, 43, 44]。研究表明, 豌豆蚜的寄主专化性有其相应的遗传学基础。例如, 豌豆蚜当地和引进种群均表现出低水平的核苷酸多样性和中低水平的连锁不平衡[45, 46]。取食不同植物的豌豆蚜, 决定其寄主植物利用和蚜虫交配选择的数量性状基因紧密连锁, 从而能够促进寄主专化和蚜虫生殖隔离的共同进化[9]。此外, 用不同的固醇类和植物饲养的豌豆蚜, 其基因表达存在差异性[47]。通过豌豆蚜唾液腺转录组基因的表达差异研究, 揭示了豌豆蚜对不同寄主植物适应性差异的分子机理[48]。

蚜虫以刺吸式口器吸取植物韧皮部汁液来获得营养, 而植物韧皮部汁液富含昆虫喜食的糖类物质[49]。通常, 豌豆蚜喜在植物茎和顶部嫩叶上取食, 对植物的生长发育具有重要的影响[19]。豌豆蚜取食紫花苜蓿的生长区时, 植物的拔节率显著降低, 而当取食成熟区时拔节率则无显著变化[50]。豌豆蚜对植物的取食作用还影响植物的同化物分配, 而豌豆蚜可通过改变自身的营养成分结构来适应植物中营养物质的变化, 从而适应新生境[34, 50]。

1.3 生殖活动

豌豆蚜是典型的世代交替昆虫, 即在食物充足、环境良好的情况下营孤雌生殖, 而在环境恶化和食物匮乏时进行有性生殖(图1)。豌豆蚜的越冬卵通常小于1 mm[16], 而其孤雌生殖的胚胎较有性生殖的卵更小[51]。在孤雌生殖的分娩期间, 从母体到第一龄若虫需约15 min[52]。豌豆蚜在适温下, 卵孵化后经过约7 d即可发育成成虫, 体长达49 mm[2, 22]。豌豆蚜雌成虫繁殖能力强, 在适温下单雌产蚜量可高达138头, 生殖期长达23个月。豌豆蚜在大约3/4的生活史中营无性生殖, 易于近亲繁殖; 但因其具有识别种群中近亲的能力, 所以并未出现种群衰退现象, 然而体色识别并非其避免近亲繁殖的有效策略[53]。

豌豆蚜的生殖受光照、温度、寄主植物状态等外界因素影响, 外界条件的变化可使其在孤雌生殖和有性生殖之间发生转换[16, 29]。豌豆蚜在夏天采取孤雌生殖和胎生的方式进行繁殖, 而夏末会进行有性繁殖, 并在夏季结束前产生耐寒的越冬卵[54]。可见, 豌豆蚜在孤雌生殖向有性生殖转变的季节性调整中, 日长和温度起到了关键作用, 但日长和温度影响豌豆蚜孤雌生殖和有性生殖之间相互转变的详细机制还未被深入研究。

1.4 多型现象

多型现象在昆虫中广泛存在, 主要有体色多型、翅多型等。豌豆蚜具有体色多态性, 分为红、绿两种色型(图2), 研究报道较多的是绿色型[12, 55, 56]。1945年, Harrington首先报道了红色型豌豆蚜[57]。在我国, 贺春贵[19]于2004年首次发现并记载了豌豆蚜的红色型。在对甘肃兰州苜蓿田的调查中发现, 红色型豌豆蚜所占比例逐年上升, 有超过绿色型的趋势[58]。

豌豆蚜体色变化受自身基因型和外界环境因素的共同调控。Caillaud和Losey[28]研究表明, 蚜虫的体色是由单一的等位基因控制, 红色型则由占优势地位的显性基因控制。进一步研究表明, 红色型豌豆蚜拥有合成类胡萝卜素的相关基因, 该基因具有编码类胡萝卜素脱氢酶的功能, 而这些基因来源于真菌基因的横向转移[11]。蚜虫内共生菌同样也参与豌豆蚜的体色多态型的变化。研究表明, 兼性共生菌立克次氏小体(Rickettsia)侵染可使红色型豌豆蚜向绿色型转变[18]。虽然共生菌是否通过调控编码类胡萝卜素合成酶的基因来影响豌豆蚜的体色尚不可知, 但可以确定的是有某种共生菌参与了豌豆蚜的体色分化。环境条件可影响蚜虫的体色, 当在寒冷的环境条件下, 蚜虫体色为绿色; 在适宜的环境条件下, 为橙色蚜虫, 而当蚜虫种群数量增多食物资源匮乏时, 则出现白色蚜虫[13, 59]。高温和低温都可诱导蚜虫体色变化:豌豆蚜在8 ℃的低温条件下几乎转变为绿色, 而高温诱导可使麦长管蚜产生红色型, 暗示豌豆蚜体色多态性可能与温度以及季节变化有关[60, 61, 62]。也有研究表明, 寄主专化性也可能是诱导豌豆蚜体色多态性的重要原因之一[63]。

图2 豌豆蚜红色型和绿色型Fig. 2 The red and green morphs of the pea aphid

豌豆蚜不同体色的个体在应对天敌等外界环境因素胁迫的能力方面存在差异[64, 65, 66]。生态学研究表明, 捕食性天敌更易捕食在绿色植物上的红色型豌豆蚜, 而寄生性天敌却优先攻击绿色型[67, 68]。两种色型的豌豆蚜对于紫外线胁迫的反应也不尽相同, 当采用紫外线对豌豆蚜进行12 h辐射胁迫时, 与绿色型蚜虫相比红色型蚜虫的生长发育明显迟缓[69]。当用杀虫剂吡虫啉处理蚜虫种群后, 红色型豌豆蚜较绿色型表现出更高的敏感性[70]。此外, 在寄主植物适应性方面, 豌豆蚜不同体色个体间存在差异, 与绿色型相比红色型具有更宽的食物生态幅, 导致其在面对抗性植物时具有较强的生活力[71, 72]。不同体色豌豆蚜体内主要营养物质含量有所不同。例如, 红色型体内含有较多的碳水化合物和脂类, 而绿色型体内蛋白质含量较高, 所以当其均处于恶劣的环境条件下时, 红色型个体则具有足够的能量产生有翅蚜进行迁飞从而逃避恶劣环境[64, 73]。不同色型间所表现出的不同生物学特性, 是豌豆蚜对整个生活史进行权衡后所呈现的一些适应性特征, 利于提高其在自然环境、特别是逆境中的适合度[74]。

豌豆蚜是典型的翅多型昆虫。豌豆蚜孤雌生殖会产生翅二型后代, 该后代可发育成有翅或无翅成蚜。有翅豌豆蚜的发生会直接影响到天敌的释放效率, 因此深入研究其翅多型产生的原因对该虫的生物防治具有十分重要的作用。豌豆蚜有翅和无翅型的形成是由环境条件和豌豆蚜自身基因型共同决定的[75], 其中种群密度和天敌是最为关键的两个外界因素。当种群密度大时, 产生有利于迁飞到其它寄主植物上取食的有翅蚜, 有翅蚜的转移危害有利于物种间的基因交流, 同时可形成新的生物型并危害新的寄主植物, 进而在一定程度上增加了寄主范围[76]。天敌因素也可诱导有翅蚜的产生[77]。天敌的存在会使豌豆蚜释放一些可诱导翅型改变的信息素, 如警报信息素等[78, 79, 80]。有翅蚜的出现同时受温度和光周期的影响, 豌豆蚜在不同的温度和光照组合下会产生有翅和无翅孤雌蚜、雄蚜和产卵雌蚜[81]。目前, 有关豌豆蚜两种翅型间转换的分子机制研究已逐渐开展。对豌豆蚜翅多型遗传基础的研究发现, 雄性豌豆蚜中与翅型相关的基因位点是伴随性别决定来进行调控的[82]。而诱导翅型发育基因的位置不仅影响雄性个体的翅型, 同样也与雌性翅的非遗传多型性相关[76]。继张传溪团队揭示胰岛素信号通路中的胰岛素受体在褐飞虱(Nilaparvata lugens)翅型形成的分子机制中发挥开关式的调节作用后[83], Guo等[84]首次对豌豆蚜胰岛素信号通路中相关基因的功能进行了研究, 发现胰岛素信号通路中的Apirp5参与了翅二型豌豆蚜的胚胎发育和代谢调节。

翅多型现象是豌豆蚜对生存环境的一种适应性表现。例如, 豌豆蚜无翅个体的卵期及世代时间明显短于有翅个体, 且拥有更高的繁殖力[75, 85]。豌豆蚜的翅型同样也会影响其交配行为和繁殖率, 在一对一的交配竞争中有翅豌豆蚜会获得较多的交配对象, 而在无竞争状态下, 无翅雄性一生中的繁殖成功率比有翅雄性稍高[86]。相对于雌性, 有翅和无翅的雄性在形态学上并不明显, 这可能是由于雄性很少在生殖和传播间进行权衡所致[87]。

1.5 内共生菌

在长期协同进化过程中, 蚜虫与其体内共生菌形成了复杂的共生关系, 共生菌与蚜虫之间密切互作、协同进化[88]。几乎所有的蚜虫都含有内共生菌, 这些细菌为同一属巴克纳氏菌(Buchnera), 称为专性共生菌(obligate symbiont)。豌豆蚜和Buchnera的共生关系可追溯到25亿年以前[89]。共生菌位于豌豆蚜腹部的含菌胞内, 这些菌胞很少分裂, 但会随着蚜虫的生长而逐渐变大[90, 91]。共生菌的数量在豌豆蚜不同生长阶段有所不同; 电镜观察发现, 豌豆蚜Buchnera数量在胚胎菌胞的形成过程中数量增加, 而在卵的形成过程中数量减少[92]。内共生菌在蚜虫寄主内是通过卵和孤雌胚胎进行垂直传播的[93]; 在进行有性生殖时, 将传递给卵细胞, 而孤雌生殖时则传递给胚胎[94]。

内共生关系一直是生物学研究的热点, 而豌豆蚜和内共生菌Buchnera的专性共生关系使其成为内共生关系研究的理想模型。随着豌豆蚜及其内共生菌Buchnera全基因组测序的完成[10, 29], 目前研究主要侧重于依赖生理和基因组数据的Buchnera-蚜虫的进化关系以及两者间的营养代谢关系[95, 96]。尽管有研究称在低级阶元水平上Buchnera-蚜虫符合平行分化关系, 但在高级阶元水平上却缺乏严格的对应关系[95]。同时又有人推测, Buchnera基因组的进化效率和横向转移可能导致Buchnera-蚜虫在高低阶元间不同的发育格局[97]。然而关于两者的进化关系仍不清楚, 大多数研究关注Buchnera-蚜虫的营养代谢关系。豌豆蚜与其共生菌共同参与某些必需氨基酸的生物合成, 且宿主蚜虫能精确地调控Buchnera的新陈代谢[98]。专性共生菌Buchnera具有维生素合成通路, 可为蚜虫提供所需维生素和腺嘌呤, 并同时利用蚜虫产生的鸟嘌呤来满足自身对于核苷酸的需求[99, 100]。

豌豆蚜除含有专性内共生菌外, 其体内还含有多种其它细菌类群, 称为次级共生菌, 又称兼性共生菌(facultative symbiont)。兼性共生菌是指部分蚜虫体内含有而另一部分蚜虫体内不含有的一类共生菌。迄今, 有关蚜虫兼性共生菌的研究中, 豌豆蚜内共生菌的研究较为深入, 目前已报道7种不同的兼性共生菌[101, 102, 103, 104](表1)。豌豆蚜每个个体可感染多达4种兼性共生菌[67, 101], 其中研究较多的是Serratia。研究发现, 次级共生菌存在于菌胞周围的鞘细胞和蚜虫血腔中[94]。通常, 次级内共生菌通过垂直方式进行传播[103]。但由于不同地理种群的蚜虫体内含有不同种类的次级内共生菌, 所以能够引起混合侵染的水平传递可能也是其主要传播方式[110]。兼性共生菌与豌豆蚜的生物生态学特性密切相关[103]。一方面, 兼性共生菌可为豌豆蚜提供营养、调控蚜虫生殖、参与蚜虫的体色变化和诱导翅型的产生[18, 109, 111]。另一方面, 共生菌能够提高蚜虫抵抗病原菌、高温、抵御天敌的能力, 同时可提高豌豆蚜对寄主植物的适应性来促进不同寄主专化型的产生[72, 88, 94, 103, 106, 107, 108, 112, 113, 114, 115]。此外, 兼性共生菌在改变豌豆蚜的免疫力过程中亦扮演着重要角色[116]。

表1 已知豌豆蚜兼性共生菌种类总结 Table 1 The summary of facultative symbionts in Acyrthosiphon pisum
2 生态学特性
2.1 温度及光照

温度是影响豌豆蚜生长发育及体色多态性的重要因素。豌豆蚜各个发育阶段的发育速率随温度的升高而加快[117, 118]; 在24 ℃条件下豌豆蚜的内禀增长率最大, 在18 ℃时具有最高的种群净增殖率, 在27 ℃时繁殖力显著下降; 在31 ℃下豌豆蚜若虫虫体很小, 能蜕皮但不能正常发育为成蚜[119]。在不同温度下饲养豌豆蚜, 发现当温度高于19.6 ℃时若蚜死亡率最高[120]。这些研究均表明, 豌豆蚜不耐高温。此外, 环境温度不仅影响豌豆蚜的生长发育, 还可以塑造豌豆蚜之间的个体差异[121]。目前, 关于温度对豌豆蚜体色的影响主要集中在低温[60], 但对于其影响豌豆蚜体色的内在分子机制尚不清楚。

豌豆蚜是一类对光照较为敏感的昆虫, 光照除了影响蚜虫的时空分布、生长发育及取食行为之外, 对豌豆蚜的生殖转变、性别分化、翅型及体色分化均造成不同程度的影响[16, 81, 122, 123]。研究还发现, 豌豆蚜因能够自身合成光合作用的重要色素类胡萝卜素, 从而具备吸收太阳光作为其代谢能量的特殊能力, 推测其为目前唯一具备光合能力的动物[60]。

2.2 杀虫剂

蚜虫每年能够造成数百亿的作物损失, 杀虫剂的使用仍然是当前控制蚜虫包括豌豆蚜最重要的手段之一[35]。控制豌豆蚜的杀虫剂主要有吡虫啉、阿维菌素、高效氯氰菊酯等[13]。豌豆蚜与其天敌昆虫均受到亚致死效应的影响, 亚致死效应对于协调化学农药防治蚜虫具有重要的作用[124, 125]。随着吡虫啉亚致死剂量的增加, 豌豆蚜F0代成蚜寿命缩短, 产蚜量减少, 且影响F1代种群的生长发育及繁殖[126]。

随着豌豆蚜绿色防治研究的不断深入, 生物农药的研究和应用越来越受到重视。蛋白酶抑制剂蛋白有防治害虫的潜质, 它可以通过抑制昆虫体内蛋白酶和淀粉酶的作用, 延迟幼虫的发育, 导致其体重减少、免疫力和生殖率降低, 最后导致昆虫死亡[14, 35]。同时受生物环境影响的昆虫激肽类似物也能够提高豌豆蚜的拒食素活性和诱发高死亡率[127, 128]等。另外, 皂苷、芹黄素糖苷在防控豌豆蚜中均有潜在应用前景[129, 130]。

2.3 天敌昆虫

天敌昆虫在豌豆蚜的控制中发挥着重要的作用, 目前已报道的豌豆蚜自然天敌来自5目7科[35, 131](表2)。

表2 已报道的豌豆蚜天敌昆虫种类 Table 2 Reported natural enemiesof Acyrthosiphon pisum

捕食性天敌和寄生性天敌在控制豌豆蚜危害方面均发挥重要作用。豌豆蚜的捕食性天敌主要有瓢虫、草蛉、蝽和食蚜蝇等, 而寄生性天敌研究相对较多的则为蚜茧蜂[132]。田间调查发现, 多异瓢虫是甘肃省苜蓿田中主要的捕食性天敌之一, 可在一定程度上减轻豌豆蚜的危害[19]。瓢虫的个体大小和龄期均能够影响其对豌豆蚜的捕食效率, 个体较大的瓢虫捕食效率较高[133], 成虫和4龄幼虫捕食作用较其它龄期强[134, 135]。七星瓢虫(Coccinella septempunctata)对豌豆蚜捕食功能反应的研究表明, 攻击率最强且处理时间最短的虫态为七星瓢虫的成虫[136]。同日龄瓢虫在豌豆蚜不同密度梯度时, 捕食量具有显著差异[136]。异色瓢虫(Harmonia axyridis)在低种群数量时, 对豌豆蚜两种色型未表现出偏好选择性, 而在较高种群数量时, 对豌豆蚜红色型表现出一定的偏好选择性[137]。大灰食蚜蝇(Metasyrphus corollae)对豌豆蚜具有较强的捕食作用[138], 而一种杂食性椿象(Macrolophus pygmaeus)对豌豆蚜也具有捕食作用[139]。

3 总结及展望

豌豆蚜不仅具有重要的经济价值, 而且还具有重要的生态学研究价值。尽管已对豌豆蚜的基础生物生态学进行了广泛研究, 但对其生态适应性、为害机理及遗传进化等方面的研究还十分欠缺。在全球气候变化和当下牧草种植结构及作物布局发生重大变化的大背景下, 需进一步深入研究豌豆蚜生物生态学特性的演变规律, 尤其要加强豌豆蚜在遗传、生理、行为等方面对环境变化响应的研究, 为控制豌豆蚜的危害提供理论依据。

豌豆蚜极高的种群密度及其危害性, 与其丰富的遗传多样性密切相关。研究豌豆蚜的种群遗传与进化, 有助于进一步深入认识豌豆蚜的生物生态学特性, 揭示种群的演化规律及生态进化过程, 也可为该虫的防控提供理论指导。我国苜蓿地豌豆蚜自然种群中红色型与绿色型的种群密度比率一直处于动态变化当中, 且近年来红色型种群数量呈逐年上升趋势。与绿色型相比, 豌豆蚜红色型在绿色植物上具有较高的可见度, 故红色型更易遭遇天敌捕食而在进化过程中处于不利地位。然而, 关于豌豆蚜两种体色型的相互转变以及自然种群相对数量的演替机制, 目前尚不清楚。

随着人们对豌豆蚜生物生态学特性研究的不断深入, 对其生态适应性遗传机制的研究变得尤为重要。翅多型和体色变化是研究其生态适应性的两个重要切入点。最近的研究[84]发现, 豌豆蚜胰岛素信号通路中的Apirp5与其翅多型密切相关, 这与褐飞虱翅型变化的研究结果类似[83], 但有关豌豆蚜翅型变化的遗传机制仍不甚清楚。研究表明, 低温可诱导豌豆蚜体色在红绿之间转变[11], 而共生菌同样也参与了豌豆蚜体色的变化[12]。因此, 豌豆蚜体色多态性可能受到诸多环境因子及自身遗传的共同作用。深入研究豌豆蚜体色变化的遗传学基础, 是今后应该重点关注的研究内容。

近年来, 豌豆蚜已从苜蓿田的次要害虫上升为主要害虫, 原本以抗苜蓿斑蚜为主的部分苜蓿品种对豌豆蚜的抗性丧失, 抗性的丧失会造成田间蚜虫的大爆发[71]。天敌防治和生物药剂防治均可作为豌豆蚜防治的有效手段[140], 而一些常用农事操作也可在一定程度上控制苜蓿田中的害虫数量[141, 142]。种植抗性品种不但可从根本上控制蚜虫的危害, 同时也可减少化学农药的使用从而达到保护天敌的目的。因此, 选育并利用抗蚜品种是防控豌豆蚜的重要途径。另外, 作物布局显著影响豌豆蚜的种群数量及季节性发生规律[23, 38]。因此, 有必要进一步探明作物布局、气候等因素对豌豆蚜种群产生的影响, 以便发展和完善不同地区不同作物上豌豆蚜的防控技术体系。综上所述, 应在深入研究豌豆蚜生物生态学特性和生态适应性机制的基础之上, 建立以利用抗蚜品种为中心, 天敌和生物防治为基础, 化学防治为辅的豌豆蚜绿色防控技术体系。

(责任编辑 王芳)

The authors have declared that no competing interests exist.

参考文献
[1] Blackman R L, Eastop V F. Aphids on the World’s Trees: An Identification and Information Guide. Wallingford, Oxon, UK: CAB International, 1994. [本文引用:1]
[2] Brisson J A, Stern D L. The pea aphid, Acyrthosiphon pisum: An emerging genomic model system for ecological, developmental and evolutionary studies. Bioessays, 2006, 28(7): 747-755. [本文引用:3]
[3] von Dohlen C D, Rowe C A, Heie O E. A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences. Molecular Phylogenetics and Evolution, 2006, 38(2): 316-329. [本文引用:1]
[4] Qiao G, Zhang G. Preliminary study of aphid diversity in China: Taxonomic and geographical variation. Aphids in a New Millennium. Paris: Institut National de la Recherché Agronomique, 2004: 139-146. [本文引用:1]
[5] Figueroa C, Simon J, Le Gallic J, Prunier L N, Briones L, Dedryver C, Niemeyer H. Genetic structure and clonal diversity of an introduced pest in Chile, the cereal aphid Sitobion avenae. Heredity, 2005, 95(1): 24-33. [本文引用:1]
[6] Guo X Z, Gaoj K, Li F J, Wang J. Evidence of horizontal transfer of non-autonomous Lep1 Helitrons facilitated by host-parasite interactions. Scientific Reports, 2014, 4: 5119. [本文引用:1]
[7] Zhao Y, Zhang S, Luo J Y, Wang C Y, Lyu L M, Wang X P, Cui J J, Lei C L. Bt proteins Cry1Ah and Cry2Ab do not affect cotton aphid Aphis gossypii and ladybeetle Propylea japonica. Scientific Reports, 2016, 6: 20368. [本文引用:1]
[8] Dáder B, Fereres A, Moreno A, Trębicki P. Elevated CO2 impacts bell pepper growth with consequences to Myzus persicae life history, feeding behaviour and virus transmission ability. Scientific Reports, 2016, 6: 19120. [本文引用:1]
[9] Hawthorne D J, Via S. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature, 2001, 412: 904-907. [本文引用:3]
[10] Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature, 2000, 407: 81-86. [本文引用:2]
[11] Moran N A, Jarvik T. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science, 2010, 328: 624-627. [本文引用:5]
[12] Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon J C, Fukatsu T. Symbiotic bacterium modifies aphid body color. Science, 2010, 330: 1102-1104. [本文引用:5]
[13] 马亚玲, 刘长仲. 蚜虫的生态学特性及其防治. 草业科学, 2014, 31(3): 519-525.
Ma Y L, Liu C Z. Review on ecological characteristics and control of aphids. Pratacultural Science, 2014, 31(3): 519-525. (in Chinese) [本文引用:4]
[14] Jin D J, Zeng F R, Dong S L, Zhang H Q. Effects of a protease inhibitor protein from Xenorhabdus bovienii on physiology of pea aphid ( Acyrthosiphon pisum). Pesticide Biochemistry and Physiology, 2014, 108: 86-91. [本文引用:3]
[15] He C, Zhang X. Field evaluation of lucerne ( Medicago sativa L. ) for resistance to aphids in northern China. Crop and Pasture Science, 2006, 57(4): 471-475. [本文引用:2]
[16] Trionnaire G, Hardie J, Jaubert P S, Simon J C, Tagu D. Shifting from clonal to sexual reproduction in aphids: Physiological and developmental aspects. Biology of the Cell, 2008, 100(8): 441-451. [本文引用:8]
[17] Nanoth Vellichirammal N, Madayiputhiya N, Brisson J A. The genome wide transcriptional response underlying the pea aphid wing polyphenism. Molecular Ecology, 2016, 25: 4146-4160. [本文引用:3]
[18] Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon J C, Fukatsu T. Symbiotic bacterium modifies aphid body color. Science, 2010, 330: 1102-1104. [本文引用:3]
[19] 贺春贵. 苜蓿病虫草鼠害防治. 北京: 中国农业出版社, 2004. [本文引用:4]
[20] Harmon J P, Moran N A, Ives A R. Species response to environmental change: Impacts of food web interactions and evolution. Science, 2009, 323: 1347-1350. [本文引用:1]
[21] 王明利. 中国牧草产业经济. 北京: 中国农业出版社, 2010.
Wang M L. China Grass Industry Economy. Beijing: China Agriculture Press, 2010. (in Chinese) [本文引用:1]
[22] 武德功. 豌豆蚜地理种群遗传多样性及其种群调控机制研究. 兰州: 甘肃农业大学硕士学位论文, 2011.
Wu D G. On genetic diversity of geographic populations of Acyrthosiphon pisum Harris (Homoptera: Aphididae) and it’s population regulating mechanism. Master Thesis. Lanzhou: Gansu Agricultural University, 2011. (in Chinese) [本文引用:4]
[23] 刘金平, 张新全, 刘瑾, 张晓琴. 苜蓿产业化生产中蚜虫危害及防治方法研究. 草业科学, 2005, 22(10): 74-77
Liu J P, Zhang X Q, Liu J, Zhang X Q. Study on the control method of aphids in alfalfa industrial production. Pratacultural Science, 2005, 22(10): 74-77. (in Chinese) [本文引用:2]
[24] Emden H F V. Aphids as Crop Pests. Berks, UK: Crownwell, 2007. [本文引用:1]
[25] Brault V, Uzest M, Monsion B, Jacquot E, Blanc S. Aphids as transport devices for plant viruses. Comptes Rendus Biologies, 2010, 333(6-7): 524-538. [本文引用:1]
[26] Seye F, Bawin T, Boukraa S. Effect of entomopathogenic Aspergillus strains against the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae). Applied Entomology & Zoology, 2014, 49(3): 453-458. [本文引用:1]
[27] Powell G, Tosh C R, Hardie J. Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annual Review of Entomology, 2006, 51: 309-330. [本文引用:1]
[28] Caillaud M C, Losey J E. Genetics of color polymorphism in the pea aphid, Acyrthosiphon pisum. Journal of Insect Science, 2010, 10: 95. [本文引用:2]
[29] Consortium I G. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biology, 2010, 8(2): e1000313. [本文引用:3]
[30] Ollivier M, Legeai F, Rispe C. Comparative analysis of the Acyrthosiphon pisum genome and expressed sequence tag-based gene sets from other aphid species. Insect Molecular Biology, 2010, 19(S2): 33-45. [本文引用:1]
[31] Tamborindeguy C, Monsion B, Brault V, Hunnicutt L, Ju H J, Nakabachi A, van Fleet E. A genomic analysis of transcytosis in the pea aphid, Acyrthosiphon pisum, a mechanism involved in virus transmission. Insect Molecular Biology, 2010, 19(S2): 259-272. [本文引用:1]
[32] Duncan E J, Leask M P, Dearden P K. The pea aphid ( Acyrthosiphon pisum) genome encodes two divergent early developmental programs. Developmental Biology, 2013, 377(1): 262-274. [本文引用:1]
[33] Jedlicka P, Jedlickova V, Lee H J. Expression of stress-related genes in the parthenogenetic forms of the pea aphid, Acyrthosiphon pisum. Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology, 2015, 180: 32-37. [本文引用:1]
[34] 朱玉永. 豌豆蚜与寄主互作关系的研究. 石河子: 石河子大学硕士学位论文, 2014.
Zhu Y Y. Study on the interrelation between pea aphid and host plant. Master Thesis. Shihezi: Xinjiang University, 2007. (in Chinese) [本文引用:3]
[35] 金丹娟. 伯氏嗜线虫致病杆菌蛋白酶抑制剂对豌豆蚜 Acythosiphon pisum Harris的杀虫活性及其作用机制. 南京: 南京农业大学硕士学位论文, 2012.
Jin D J. Biological activity and the mechanism of a protease inhibitor from Xenorhabdus bovienii strain BJFS526 against pea aphid ( Acythosiphon pisum Harris). Master Thesis. Nanjing: Nanjing Agricultural University, 2012. (in Chinese) [本文引用:4]
[36] Tagu D, Le Trionnaire G, Tanguy S, Gauthier J P, Huynh J R. EMS mutagenesis in the pea aphid Acyrthosiphon pisum. G3: Genes, Genomes, Genetics, 2014, 4(4): 657-667. [本文引用:1]
[37] Friedemann K, Kunert G, Gorb E, Gorb S N, Beutel R G. Attachment forces of pea aphids ( Acyrthosiphon pisum) on different legume species. Ecological Entomology, 2015, 40(6): 732-740. [本文引用:1]
[38] 韩秀楠. 不同豆科植物对豌豆蚜生长发育和繁殖的影响. 兰州: 甘肃农业大学硕士学位论文, 2011.
Han X N. Effects of the growth, development and fccundity of Acyrthosiphon pisum Harrison different leguminous plants. Master Thesis. Lanzhou: Gansu Agricultural University, 2011. (in Chinese) [本文引用:3]
[39] Ferrari J, Godfray H C J, Faulconbridge A S, Prior K, Via S. Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera. Evolution, 2006, 60(8): 1574-1584. [本文引用:1]
[40] Mcvean R I K, Dixon A F G. The effect of plant drought-stress on populations of the pea aphid Acyrthosiphon pisum. Ecological Entomology, 2001, 26(4): 440-443. [本文引用:1]
[41] Via S. Reproductive isolation between sympatric races of pea aphids. Ⅰ. Gene flow restriction and habitat choice. Evolution, 1999, 54(5): 1446-1457. [本文引用:1]
[42] Via S. Sympatric speciation in animals: The ugly duckling grows up. Trends in Ecology and Evolution, 2001, 16(7): 381-390. [本文引用:1]
[43] Hawthorne D J, Via S. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature, 2001, 412: 904-907. [本文引用:1]
[44] Leonardo T E, Muiru G T. Facultative symbionts are associated with host plant specialization in pea aphid populations. Proceedings of the Royal Society B Biological Sciences, 2003, 270(S2): 209-212. [本文引用:1]
[45] Brisson J A, Nuzhdin S V, Stern D L. Similar patterns of linkage disequilibrium and nucleotide diversity in native and introduced populations of the pea aphid, Acyrthosiphon pisum. BMC Genetics, 2009, 10: 22. [本文引用:1]
[46] Jean P, Jean Christophe S. The pea aphid complex as a model of ecological speciation. Ecological Entomology, 2010, 35(S1): 119-130. [本文引用:1]
[47] Bouvaine S, Behmer S T, Lin G G, Faure M L, Grebenok R J, Douglas A E. The physiology of sterol nutrition in the pea aphid Acyrthosiphon pisum. Journal of Insect Physiology, 2012, 58(11): 1383-1389. [本文引用:1]
[48] Lu H, Yang P C, Xu Y Y, Luo L, Zhu J J, Cui N, Kang L, Feng C. Performances of survival, feeding behavior, and gene expression in aphids reveal their different fitness to host alteration. Scientific Reports, 2015, 6(1): 19344. [本文引用:1]
[49] Douglas A E, Price D R G, Minto L B, Jones E, Pescod K V, Francois C, Pritchard J, Boonham N. Sweet problems: insect traits defining the limits to dietary sugar utilisation by the pea aphid, Acyrthosiphon pisum. Journal of Experimental Biology, 2006, 209(8): 1395-1403. [本文引用:1]
[50] Girousse C, Faucher M, Kleinpeter C, Bonnemain J L. Dissection of the effects of the aphid Acyrthosiphon pisum feeding on assimilate partitioning in Medicago sativa. New Phytologist, 2003, 157(1): 83-92. [本文引用:2]
[51] Miura T, Braendle C, Shingleton A, Sisk G, Kambhampati S, Stern D L. A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2003, 295(1): 59-81. [本文引用:1]
[52] Greven H, Lindermann S. Notes on the birth process in the aphid species Acyrthosiphon pisum and Aphis fabae (Sternorrhyncha: Aphididae). Entomologia Generalis, 2005, 27(3-4): 211-222. [本文引用:1]
[53] Huang M H, Caillaud M C. Inbreeding avoidance by recognition of close kin in the pea aphid, Acyrthosiphon pisum. Joural of Insect Science, 2012, 12: 39. [本文引用:1]
[54] Smith M H, Mackay P A, Lamb R J. Temperature modulation of photoperiodism and the timing of late-season changes in life history for an aphid, Acyrthosiphon pisum. Canadian Entomologist, 2011, 143(1): 56-71. [本文引用:1]
[55] Shigenobu S, Bickel R D, Brisson J A, Butts T, Chang C C, Christiaens O, Davis G K, Duncan E J, Ferrier D E K, Iga M, Janssen R, Lin G W, Lu H L, Mcgregor A P, Miura T, Smagghe G, Smith J M, van der Zee M, Velarde R A, Wilson M J, Dearden P K, Stern D L. Comprehensive survey of developmental genes in the pea aphid, Acyrthosiphon pisum: Frequent lineage-specific duplications and losses of developmental genes. Insect Molecular Biology, 2010, 19(S2): 47-62. [本文引用:1]
[56] 王小强, 韩秀楠, 曹馨月, 张廷伟, 刘长仲. 豌豆品种对绿色型豌豆蚜种群参数的影响. 中国生态农业学报, 2013, 21(8): 1004-1008.
Wang X Q, Han X N, Cao X Y, Zhang T W, Liu C Z. Effects of different garden pea cultivars on population parameters of the green morph of pea aphid, Acyrthosiphon pisum. Chinese Journal of Eco-Agriculture, 2013, 21(8): 1004-1008. (in Chinese) [本文引用:1]
[57] Harrington C. Biological races of the pea aphid. Journal of Economic Entomology, 1945, 38(1): 12-22. [本文引用:1]
[58] 杜军利. 两种色型豌豆蚜种群数量变化机制研究. 兰州: 甘肃农业大学博士学位论文, 2013.
Du J L. Study on the changes mechanism of quantity of population of two color morphs pea aphid Acyrthosiphon pisum. PhD Thesis. Lanzhou: Gansu Agricultural University, 2013. (in Chinese) [本文引用:1]
[59] Baeza G A, Pierce R J, Gourbal B, Werkmeister E, Colinet D, Reichhart J M, Dissous C, Coustau C. Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathogens, 2010, 6(9): e1001115. [本文引用:1]
[60] Valmalette J C, Dombrovsky A, Brat P, Mertz C, Capovilla M, Robichon A. Light-induced electron transfer and ATP synthesis in a carotene synthesizing insect. Scientific Reports, 2012, 2(2): 00579. [本文引用:3]
[61] 邓明明, 高欢欢, 李丹, 胡想顺, 胡祖庆, 赵惠燕. 温度对麦长管蚜体色变化的影响. 生态学报, 2011, 31(23): 7203-7210.
Deng M M, Gao H H, Li D, Hu X S, Hu Z Q, Zhao H Y. Effects of temperature on body color in Sitobion avenae (F. ). Acta Ecologica Sinica, 2011, 31(23): 7203-7210. (in Chinese) [本文引用:1]
[62] Takada H. Inheritance of body colors in Myzus persicae (SULZER) (Homoptera: Aphididae). Applied Entomology & Zoology, 1981, 16(3): 242-246. [本文引用:1]
[63] Peccoud J, Simon J C. The pea aphid complex as a model of ecological speciation. Ecological Entomology, 2010, 35(S1): 119-130. [本文引用:1]
[64] Braendle C, Weisser W W. Variation in escape behavior of red and green clones of the pea aphid. Journal of Insect Behavior, 2001, 14(4): 497-509. [本文引用:2]
[65] Farhoudi F, Allahyari H, Tabadkani S M, Gholizadeh M. Prey preference of Aphidoletes aphidimyza on Acyrthosiphon pisum: Effect of prey color and size. Journal of Insect Behavior, 2014, 27(6): 776-785. [本文引用:1]
[66] Losey J E, Harmon J, Ballantyne F, Brown C. A polymorphism maintained by opposite patterns of parasitism and predation. Nature, 1997, 388: 269-272. [本文引用:1]
[67] Frantz A, Calcagno V, Mieuzet L, Plantegenest M, Simon J C. Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): Implications for the evolution of ecological specialisation. Biological Journal of the Linnean Society, 2009, 97(4): 718-727. [本文引用:2]
[68] Libbrecht R, Gwynn D M, Fellowes M D E. Aphidius ervi preferentially attacks the green morph of the pea aphid, Acyrthosiphon pisum. Journal of Insect Behavior, 2007, 20(1): 25-32. [本文引用:1]
[69] 杜军利, 武德功, 张廷伟, 钱秀娟, 刘长仲. 紫外线 (UV-B) 辐射对不同色型豌豆蚜生物学特性的影响. 中国生态农业学报, 2012, 20(12): 1626-1630.
Du J L, Wu D G, Zhang T W, Qian X J, Liu C Z. Effect of UV-B for different radiation durations on biological characteristics of two color morphs of pea aphid Acyrthosiphon pisum(Harris) offspring. Acta Agrestia Sinica, 2012, 20(12): 1626-1630. (in Chinese) [本文引用:1]
[70] 王小强, 刘长仲, 祁发鹏, 李毅恒. 吡虫啉亚致死剂量对2种色型豌豆蚜生长发育和种群参数的影响. 草地学报, 2014, 22(5): 1110-1116.
Wang X Q, Liu C Z, Qi F P, Li Y H. Effects of sublethal dosage of imidacloprid on the growth, development and population parameter of two color morphs of pea aphid. Acta Agrectia Sinica, 2014, 22(5): 1110-1116. (in Chinese) [本文引用:1]
[71] Kugler J, Ratcliffe R. Resistance in alfalfa to a red form of the pea aphid (Homoptera: Aphididae). Journal of Economic Entomology, 1983, 76(1): 74-76. [本文引用:2]
[72] Simon J C, Carre S, Boutin M, Prunier-Leterme N, Sabater-Muñoz B, Latorre A, Bournoville R. Host-based divergence in populations of the pea aphid: Insights from nuclear markers and the prevalence of facultative symbionts. Proceedings of the Royal Society of London B: Biological Sciences, 2003, 270: 1703-1712. [本文引用:2]
[73] Ahsaei S M, Tabadkani S M, Hosseininaveh V, Allahyari H, Bigham M. Differential accumulation of energy by the colour morphs of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) mirrors their ecological adaptations. European Journal of Entomology, 2013, 110(2): 241-245. [本文引用:1]
[74] Schuett W, Dall S R, Kloesener M H, Baeumer J, Beinlich F, Eggers T. Life-history trade-offs mediate ‘personality’ variation in two colour morphs of the pea aphid, Acyrthosiphon pisum. Journal of Animal Ecology, 2015, 84(1): 90-101. [本文引用:1]
[75] Ogawa K, Ishikawa A, Kanbe T, Akimoto S, Miura T. Male-specific flight apparatus development in Acyrthosiphon pisum (Aphididae, Hemiptera, Insecta): Comparison with female wing polyphenism. Zoomorphology, 2012, 131(3): 197-207. [本文引用:2]
[76] Braendle C, Caillaud M C, Stern D L. Genetic mapping of aphicarus——A sex-linked locus controlling a wing polymorphism in the pea aphid ( Acyrthosiphon pisum). Heredity, 2005, 94(4): 435-442. [本文引用:2]
[77] Sloggett J J, Weisser W W. Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum. Oikos, 2002, 98(2): 323-333. [本文引用:1]
[78] Kunert G, Trautsch J, Weisser W W. Density dependence of the alarm pheromone effect in pea aphids, Acyrthosiphon pisum (Sternorrhyncha: Aphididae). European Journal of Entomology, 2007, 104(1): 47-50. [本文引用:1]
[79] Schwartzberg E G, Kunert G, Roese U S R, Gershenzon J, Weisser W W. Alarm pheromone emission by pea aphid, Acyrthosiphon pisum, clones under predation by lacewing larvae. Entomologia Experimentalis et Applicata, 2008, 128(3): 403-409. [本文引用:1]
[80] Schwartzberg E G, Kunert G, Westerlund S A, Hoffmann K H, Weisser W W. Juvenile hormone titres and winged offspring production do not correlate in the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 2008, 54(9): 1332-1336. [本文引用:1]
[81] 刘向东, 翟保平, 张孝羲. 蚜虫迁飞的研究进展. 昆虫知识, 2004, 41(4): 301-307.
Liu X D, Zhai B P, Zhang X X. Advance in the studies of migration of aphids. Entomological Knowledge, 2004, 41(4): 301-307. (in Chinese) [本文引用:2]
[82] Caillaud M C, Boutin M, Braendle C, Simon J C. A sex-linked locus controls wing polymorphism in males of the pea aphid, Acyrthosiphon pisum (Harris). Heredity, 2002, 89(5): 346-352. [本文引用:1]
[83] Xu H J, Xue J, Lu B, Zhang X C, Zhuo J C, He S F, Ma X F, Jiang Y Q, Fan H W, Xu J Y. Two insulin receptors determine alternative wing morphs in planthoppers. Nature, 2015, 519: 464-467. [本文引用:2]
[84] Guo S S, Zhang M, Liu T X. Insulin-related peptide 5 is involved in regulating embryo development and biochemical composition in pea aphid with wing polyphenism. Frontiers in Physiology, 2016, 7: 31. [本文引用:2]
[85] Müller C B, Williams I S, Hardie J. The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology, 2001, 26(3): 330-340. [本文引用:1]
[86] Sack C, Stern D L. Sex and death in the male pea aphid, Acyrthosiphon pisum: The life-history effects of a wing dimorphism. Journal of Insect Science, 2007, 7: 1-9. [本文引用:1]
[87] Zera A J, Denno R F. Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology, 1997, 42(1): 207-230. [本文引用:1]
[88] Tsuchida T, Koga R, Fukatsu T. Host plant specialization governed by facultative symbiont. Science, 2004, 303: 1989. [本文引用:2]
[89] Moran N A, Munson M A, Baumann P, Ishikawa H. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proceedings of the Royal Society of London B: Biological Sciences, 1993, 253: 167-171. [本文引用:1]
[90] Baumann P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology, 2005, 59: 155-189. [本文引用:1]
[91] Douglas A. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology, 1998, 43(1): 17-37. [本文引用:1]
[92] Mira A, Moran N. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microbial Ecology, 2002, 44(2): 137-143. [本文引用:1]
[93] Werren J H, Baldo L, Clark M E. Wolbachia: Master manipulators of invertebrate biology. Nature Reviews Microbiology, 2008, 6(10): 741-751. [本文引用:1]
[94] Fukatsu T, Nikoh N, Kawai R, Koga R. The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Applied and Environmental Microbiology, 2000, 66(7): 2748-2758. [本文引用:3]
[95] 刘琳, 黄晓磊, 乔格侠. 蚜虫初级内共生菌 Buchnera aphidicola研究进展. 应用昆虫学报, 2013, 50(5): 1419-1427.
Liu L, Huang X L, Qiao G X. Trends in research on the primary endosymbiont of aphids, Buchnera aphidicola. Chinese Journal of Applied Entomology, 2013, 50(5): 1419-1427. (in Chinese) [本文引用:2]
[96] Nikoh N, Mccutcheon J P, Kudo T, Miyagishima S Y, Moran N A, Nakabachi A. Bacterial genes in the aphid genome: Absence of functional gene transfer from Buchnera to its host. PLoS Genetics, 2010, 6(2): e1000827. [本文引用:1]
[97] 黄晓磊, 刘琳, 乔格侠. 蚜虫与其初级内共生菌进化关系: 假说及演化机理. 昆虫学报, 2011, 54(5): 582-588.
Huang X L, Liu L, Qiao G X. Evolutionary relationships between aphids and their primary endosymbionts: Hypotheses and evolution mechanisms. Acta Entomologica Sinica, 2011, 54(5): 582-588. (in Chinese) [本文引用:1]
[98] Wilson A C C, Ashton P D, Calevro F, Charles H, Colella S, Febvay G, Jand er G, Kushlan P F, Macdonald S J, Schwartz J F, Thomas G H, Douglas A E. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Molecular Biology, 2010, 19(S2): 249-258. [本文引用:1]
[99] Moran N A, Degnan P H. Functional genomics of Buchnera and the ecology of aphid hosts. Molecular Ecology, 2006, 15(5): 1251-1261. [本文引用:1]
[100] Ramsey J S, Macdonald S J, Jand er G, Nakabachi A, Thomas G H, Douglas A E. Genomic evidence for complementary purine metabolism in the pea aphid, Acyrthosiphon pisum, and its symbiotic bacterium Buchnera aphidicola. Insect Molecular Biology, 2010, 19(S2): 241-248. [本文引用:1]
[101] Ferrari J, West J A, Via S, Godfray H C J. Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution, 2012, 66(2): 375-390. [本文引用:2]
[102] Russell J A, Weldon S, Smith A H, Kim K L, Hu Y, Łukasik P, Doll S, Anastopoulos I, Novin M, Oliver K M. Uncovering symbiont-driven genetic diversity across North American pea aphids. Molecular Ecology, 2013, 22(7): 2045-2059. [本文引用:1]
[103] Oliver K M, Degnan P H, Burke G R, Moran N A. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology, 2010, 55: 247-266. [本文引用:4]
[104] Sand ström J P, Russell J A, White J P, Moran N A. Independent origins and horizontal transfer of bacterial symbionts of aphids. Molecular Ecology, 2001, 10(1): 217-228. [本文引用:1]
[105] Oliver K M, Russell J A, Moran N A, Hunter M S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of USA, 2003, 100(4): 1803-1807. [本文引用:1]
[106] Montllor C B, Maxmen A, Purcell A H. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entomology, 2002, 27(2): 189-195. [本文引用:1]
[107] Scarborough C L, Ferrari J, Godfray H. Aphid protected from pathogen by endosymbiont. Science, 2005, 310: 1778-1781. [本文引用:1]
[108] Parker B J, Spragg C J, Altincicek B, Gerardo N M. Symbiont-mediated protection against fungal pathogens in pea aphids: A role for pathogen specificity. Applied and Environmental Microbiology, 2013, 79(7): 2455-2458. [本文引用:1]
[109] Simon J C, Boutin S, Tsuchida T, Koga R, Le Gallic J F, Frantz A, Outreman Y, Fukatsu T. Facultative symbiont infections affect aphid reproduction. PLoS One, 2011, 6(7): e21831. [本文引用:1]
[110] Moran N A, Dunbar H E. Sexual acquisition of beneficial symbionts in aphids. Proceedings of the National Academy of Sciences of USA, 2006, 103(34): 12803-12806. [本文引用:1]
[111] Leonardo T E, Mondor E B. Symbiont modifies host life-history traits that affect gene flow. Proceedings of the Royal Society of London B: Biological Sciences, 2006, 273: 1079-1084. [本文引用:1]
[112] Brady C M, Asplen M K, Desneux N, Heimpel G E, Hopper K R, Linnen C R, Oliver K M, Wulff J A, White J A. Worldwide populations of the aphid Aphis craccivora are infected with diverse facultative bacterial symbionts. Microbial Ecology, 2014, 67(1): 195-204. [本文引用:1]
[113] 吕仲贤, 俞晓平, 陈建明, 郑许松, 徐红星, 陶林勇. 共生菌在褐飞虱致害性变化中的作用. 昆虫学报, 2001, 44(2): 197-204.
Lyu Z X, Yu X P, Chen J M, Zheng X S, Xu H X, Tao L Y. Role of endosymbiote in virulence change of the brown planthopper to rice resistant varieties. Acta Entomologica Sinica, 2001, 44(2): 197-204. (in Chinese) [本文引用:1]
[114] Tegelberg R, Julkunen T R. Quantitative changes in secondary metabolites of dark-leaved willow ( Salix myrsinifolia) exposed to enhanced ultraviolet-B radiation. Physiologia Plantarum, 2001, 113(4): 541-547. [本文引用:1]
[115] Peccoud J, Ollivier A, Plantegenest M, Simon J C. A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proceedings of the National Academy of Sciences of USA, 2009, 106(18): 7495-7500. [本文引用:1]
[116] Laughton A M, Garcia J R, Gerardo N M. Condition-dependent alteration of cellular immunity by secondary symbionts in the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 2016, 86: 17-24. [本文引用:1]
[117] 高有华, 刘长仲. 豆无网长管蚜的发育起点温度和有效积温测定. 草原与草坪, 2007(2): 25-27.
Gao Y H, Liu C Z. Threshold temperature and effective accumulated temperature for Acyrthosiphon pisum development. Grassland and Turf, 2007(2): 25-27. (in Chinese) [本文引用:1]
[118] 高有华, 刘长仲. 不同温度下的豌豆蚜实验种群生命表研究. 植物保护, 2008, 34(4): 57-59.
Gao Y H, Liu C Z. Life table of the experimental population of Acyrthosiphon pisum (Harris) at different temperatures. Plant Protection, 2008, 34(4): 57-59. (in Chinese) [本文引用:1]
[119] 宫亚军, 石宝才, 路虹, 张胜利, 魏蕾. 温度对 3 种蚜虫生长发育及繁殖的影响. 华北农学报, 2006, 21(5): 96-98.
Gong Y J, Shi B C, Lu H, Zhang S L, Wei L. Effects of temperatures on the development and fecundity of three species of aphids. Journal of Agriculture in North China, 2006, 21(5): 96-98. (in Chinese) [本文引用:1]
[120] Morgan D, Walters K F A, Aegerter J N. Effect of temperature and cultivar on pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae) life history. Bulletin of Entomological Research, 2001, 91(1): 47-52. [本文引用:1]
[121] Schuett W, Dall S R X, Baeumer J, Kloesener M H, Nakagawa S, Beinlich F, Eggers T. “Personality” variation in a clonal insect: The pea aphid, Acyrthosiphon pisum. Developmental Psychobiology, 2011, 53(6): 631-640. [本文引用:1]
[122] Smith M A H, Mackay P A, Lamb R J. Temperature modulation of photoperiodism: An adaptation for long-distance dispersal in the aphid, Acyrthosiphon pisum (Hemiptera: Aphididae). Canadian Entomologist, 2013, 145(3): 302-316. [本文引用:1]
[123] 马亚玲, 刘长仲. 光周期对两种色型豌豆蚜种群参数的影响. 生态学杂志, 2016, 36(14): 4548-4555.
Ma Y L, Liu C Z. Effect of photoperiod on population parameters of two color morphs of the pea aphid Acyrthosiphon pisum. Acta Ecologica Sinica, 2016, 36(14): 4548-4555. (in Chinese) [本文引用:1]
[124] Zhang F, Sun G, Li J, Zhang Z, Piao Y, Wu J. A preliminary study on the cooridinating Trichogramma and pesticide to control Helicoverpa armigera in the cotton field. Proceedings of National Symposium on IPM in China. Beijing, China: China Agricultural Press, 1996: 6-12. [本文引用:1]
[125] 王小强, 刘长仲, 邢亚田, 石周. 吡虫啉、阿维菌素和高效氯氰菊酯亚致死剂量对绿色型豌豆蚜发育及繁殖的影响. 草业学报, 2014, 23(5): 279-286.
Wang X Q, Liu C Z, Xing Y T, Shi Z. Effects of sublethal dosage of imidacloprid, abamectin and beta-cypermethrin on the development and reproduction of green of the morph of aphid ( Acyrthosiphon pisum). Acta Prataculturae Sinica, 2014, 23(5): 279-286. (in Chinese) [本文引用:1]
[126] 惠婧婧, 刘长仲, 孟银凤, 陈洁. 吡虫啉对豌豆蚜的亚致死效应. 植物保护, 2009, 35(5): 86-88.
Hui J J, Liu C Z, Meng Y F, Chen J. Sublethal effects of imidacloprid to Acyrthosiphon pisum. Plant Protection, 2009, 35(5): 86-88. (in Chinese) [本文引用:1]
[127] Smagghe G, Mand ian K, Zubrzak P, Nachman R J. Antifeedant activity and high mortality in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidae) induced by biostable insect kinin analogs. Peptides, 2010, 31(3): 498-505. [本文引用:1]
[128] Down R E, Matthews H J, Audsley N. Effects of Mand uca sexta allatostatin and an analog on the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) and degradation by enzymes from the aphid gut. Peptides, 2010, 31(3): 489-497. [本文引用:1]
[129] Sylwia G, Leszczynski B, Wieslaw O. Effect of low and high-saponin lines of alfalfa on pea aphid. Journal of Insect Physiology, 2006, 52(7): 737-743. [本文引用:1]
[130] Golawska S, Lukasik I, Golawski A, Kapusta I, Jand a B. Alfalfa ( Medicago sativa L. ) apigenin glycosides and their effect on the pea aphid ( Acyrthosiphon pisum). Polish Journal of Environmental Studies, 2010, 19(5): 913-919. [本文引用:1]
[131] 张蓉, 马建华, 杨芳, 常兆斌, 李云, 王秉锋, 杨涛. 宁夏苜蓿害虫天敌种类及其田间发生规律的初步研究. 草业科学, 2003, 20(7): 60-62.
Zhang R, Ma J H, Yang F, Chang Z B, Li Y, Wang B F, Yang T. Preliminary study on predator species and their occurrence regulation of alfalfa insects. Pratacultural Science, 2003, 20(7): 60-62. (in Chinese) [本文引用:1]
[132] 张奔, 周敏强, 王娟, 蒲毅, 张丽, 袁明龙. 我国苜蓿害虫种类及研究现状. 草业科学, 2016, 33(4): 785-812.
Zhang B, Zhou M Q, Wang J, Pu Y, Zhang L, Yuan M L. Species checklist and research status of alfalfa insect pests reported in China. Pratacultural Science, 2016, 33(4): 785-812. (in Chinese) [本文引用:1]
[133] Mishra G, Kumar B, Shahid M, Singh D O. Evaluation of four co-occurring ladybirds for use as biocontrol agents of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). Biocontrol Science and Technology, 2011, 21(8): 991-997. [本文引用:1]
[134] 武德功, 杜军利, 刘长仲, 胡桂馨, 王森山, 贺春贵. 不同龄期龟纹瓢虫对豌豆蚜的捕食功能反应. 草地学报, 2012, 20(4): 778-783.
Wu D G, Du J L, Liu C Z, Hu G X, Wang S S, He C G. Prey response of Propylaea japonica in different instars to Acyrthosiphon pisum under growth chamber condition. Acta Agrestia Sinica, 2012, 20(4): 778-783. (in Chinese) [本文引用:1]
[135] 高有华, 刘长仲. 多异瓢虫对豆无网长管蚜捕食作用研究. 植物保护, 2007, 32(6): 51-53.
Gao Y H, Liu C Z. Studies on the predatory function of Hippodamia (Adonia) variegata (Goeze) to Acyrthosiphon pisum (Harris). Plant Protection, 2006, 32(6): 51-53. (in Chinese) [本文引用:1]
[136] Wu D G, Du J L, Liu C Z, Hu G X, Wang S S, He C G. Prey responses of propylaea japonicain different instars to Acyrthosiphon pisum under growth chamber condition. Acta Agrestia Sinica, 2012, 20(4): 778-783. [本文引用:2]
[137] 杜军利, 武德功, 刘长仲. 异色瓢虫和多异瓢虫对两种色型豌豆蚜的捕食偏好研究. 中国生态农业学报, 2015, 23(1): 102-109.
Du J L, Wu D G, Liu C Z. Study on predation preference of Harmonia axyridis(Pallas) and Adonia variegata, 2015, 23(1): 102-109. (in Chinese) [本文引用:1]
[138] 李学燕, 罗佑珍. 大灰食蚜蝇对3种蚜虫的捕食作用研究. 云南农业大学学报, 2001, 16(2): 102-104.
Li X Y, Luo Y Z. Study on the predation of Syrphus corollae Fabricius to three aphids. Journal of Yunnan Agricultural University, 2001, 16(2): 102-104. (in Chinese) [本文引用:1]
[139] Prieto J D, Trotta V, Fanti P, Casta C, Battaglia D. Predation by Macrolophus pygmaeus (Hemiptera: Miridae) on Acyrthosiphon pisum (Hemiptera: Aphididae): Influence of prey age/size and predator’s intraspecific interactions. European Journal of Entomology, 2016, 113: 37-43. [本文引用:1]
[140] 赵天璇, 袁明龙. 我国异色瓢虫的生物生态学特性. 草业科学, 2017, 34(3): 614-629.
Zhao T X, Yuan M L. Biological and ecological characteristics of Harmonia axyridis in China. Pratacultural Science, 2017, 34(3): 614-629. (in Chinese) [本文引用:1]
[141] Liu C, Zhou S. Cutting effects on the insect community structure and dynamics of alfalfa pasture. Acta Ecologica Sinica, 2003, 24(3): 542-546. [本文引用:1]
[142] 刘长仲, 严林, 魏列新, 张方, 钱秀娟. 刈割对苜蓿主要害虫种群数量动态的影响. 应用生态学报, 2008, 19(3): 691-694.
Liu C Z, Yan L, Wei L X, Zhang F, Qian X J. Effects of cutting on the population dynamics of main insect pests on alfalfa. Chinese Journal of Applied Ecology, 2008, 19(3): 691-694. (in Chinese) [本文引用:1]