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Volume 31 Issue 1
Jul.  2019
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A Review on Mud-puddling Behavior of Herbivorous Arthropods

  • The behavior of feeding and reproduction of herbivorous arthropods have received much attention from behavioral ecologists and evolutional biologists. The mud-puddling behavior, including feeding on mud, various excrements and secretions of vertebrates, and carrion, is thought to be a special behavior of supplementary feeding in lepidopteran arthropods. With the introduction of various hypotheses, the occurrence mechanism of mud-puddling has become one of the hot topics in behavioral ecology and evolutional biology. Though a wealth of observations have been added to literature, the controversies still exist mainly due to lack of convincing experimental data demonstrating the underlying mechanisms. This paper briefly reviews the history of the research on the behavior of insects, introduces the hypotheses of sex and age differentials and the driving mechanisms of mud-puddling of phytophagous herbivores, discusses the effect of this behavior on the ecological fitness and reproduction, and presents the suggestions on the methodology of future's study.
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A Review on Mud-puddling Behavior of Herbivorous Arthropods

    Corresponding author: WANG Hao-jie, haojie_wang@163.com
  • Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou 311400, Zhejiang, China

Abstract: The behavior of feeding and reproduction of herbivorous arthropods have received much attention from behavioral ecologists and evolutional biologists. The mud-puddling behavior, including feeding on mud, various excrements and secretions of vertebrates, and carrion, is thought to be a special behavior of supplementary feeding in lepidopteran arthropods. With the introduction of various hypotheses, the occurrence mechanism of mud-puddling has become one of the hot topics in behavioral ecology and evolutional biology. Though a wealth of observations have been added to literature, the controversies still exist mainly due to lack of convincing experimental data demonstrating the underlying mechanisms. This paper briefly reviews the history of the research on the behavior of insects, introduces the hypotheses of sex and age differentials and the driving mechanisms of mud-puddling of phytophagous herbivores, discusses the effect of this behavior on the ecological fitness and reproduction, and presents the suggestions on the methodology of future's study.

  • 营养与生殖是自然界生物生存繁衍的永恒主题,在长期的进化过程中,不同昆虫或同种昆虫的雌雄个体各自形成了特定的行为来完成营养摄取,实现种群繁衍[1-2]。对昆虫寄主选择、生殖等特定行为的研究为探索和理解昆虫与环境间互作的生态机制及协同进化过程创造了独特途径,同时也可为发展害虫行为调控的策略和方法提供了新的思路,因此昆虫特定行为的研究一直是昆虫学研究的重点和热点[3]

    “趋泥”(mud-puddling)行为是热带和亚热带地区蝶、蛾类鳞翅目(Lepidoptera)昆虫中一种较为常见的成虫聚集行为。迄今为止,国内外学者已对大量昆虫的趋泥行为进行了报道[4-7],但对于“昆虫为何趋泥?” “什么样的昆虫要趋泥?” “趋泥行为的生态学意义是什么?”等一系列关于昆虫趋泥行为的核心问题的回答是争论多于结论[7]。近年来,随着国内外学者对于昆虫趋泥行为研究的深入,与其相关的行为、生理及生态机制等领域均有一些新的进展[7-11],本文将对昆虫趋泥行为的研究历史、驱动力机制、泥源搜索机制及生理生态适应性等方面的研究进展进行综述,以为这一特定行为的研究提供参考。

1.   趋泥行为的定义
  • 在自然界中,常见一些蝴蝶成虫趋向并聚集于湿润的泥沙或浅水洼周围吸食(图 1A),Norris于1936年将其现象定义为“趋泥”行为。该行为在蝶、蛾类鳞翅目(Lepidoptera)昆虫中较为普遍,迄今报道有该行为的蝶、蛾类昆虫已超过100种,主要集中于凤蝶科(Papilionidae)、蛱蝶科(Nymphalidae)、弄蝶科(Hesperiidae)、灰蝶科(Lycaenidae)及尺蛾科(Geometridae),螟蛾科(Pyralidae)等21个科[12-19],“趋泥”的对象由原来的湿泥沙拓展到动物眼泪、汗液、唾液、粪便和尸体腐烂液等。趋泥行为主要发生在鳞翅目昆虫中,而在膜翅目(Hymenoptera)、同翅目(Homoptera)昆虫中也发现类似现象[20-21],如蜜蜂、汗蜂(Lisotrigona cacciae)和无刺蜂(Pariotrigona klossi)等昆虫有取食汗液和动物眼泪的习性。目前,关于昆虫趋泥行为的研究报道仅限于吸收式口器(虹吸式、刺吸式或嚼吸式)昆虫,因而趋泥行为一度被认为是吸收式口器昆虫的特有行为[7-8]

    Figure 1.  Examples of puddlers from a variety of taxa (A) Butterflies (Papilio bianor and P. xuthus) puddling on wet mud; (B) Locusts (Ceracris kiangsu) feeding on human urine

    近年来,对直翅目(Orthoptera)昆虫黄脊竹蝗(Ceracris kiangsu)的研究发现,在我国南方地区,黄脊竹蝗成虫(每年7—9月)对汗液和发酵尿液有极显著的取食偏好,并于2009年报道了首例咀嚼式口器昆虫的“趋泥”行为[7, 22](图 1B)。此外,发现部分蚂蚁种群(Hymenoptera: Formicidae)偏好取食含有盐分的诱饵,推测其可能发生趋泥行为[23],但尚未有直接试验数据证实。发生趋泥行为的昆虫类群超出了“吸收式”口器昆虫的范畴。

    发生趋泥行为被认为是昆虫补充食物营养的一种形式,目的是获取微量元素,是一种典型的补充营养行为[7-8]。双翅目中的蝇类也经常被发现附着在粪便、腐烂物、汗液和哺乳类动物的眼泪上[21]。但是这种行为很少被认为是“趋泥”,因为所取食的物质对于苍蝇来说是为最主要的食物来源,是一种取食行为[24-25],而不属于补充营养的范围。同样,把粪便和腐败物作为主要食物的昆虫的取食行为也不被认为是趋泥行为,如蜣螂、无刺蜂属中的几种蜂[26]

2.   趋泥行为与虫龄及性别的关系
  • 幼虫(若虫)及成虫因口器或习性的不同导致取食行为截然不同,成虫期因性成熟的时间与虫龄及性别密切相关,因而导致补充营养的行为有所差异[13]。学者认为,鳞翅目昆虫幼虫阶段的主要任务是取食,幼虫大量取食植物组织以完成蜕皮和生长发育,而成虫期的主要任务是生殖,成虫需要补充盐分或氮素来实现性成熟或成功交配,趋泥行为作为昆虫补充钠盐等微量元素的重要途径,主要发生在成虫阶段[8]

    动物需要钠盐用于完成很多生理功能,包括渗透调节和神经肌肉活力,而植物组织内钠盐含量远低于动物组织[23, 27-28],植食性昆虫所需钠盐比幼虫阶段取食所获得的要多[29-31],特别是鳞翅目昆虫幼虫阶段矿物质存储往往是受到限制的。同时,氮素对于昆虫生殖至关重要,但寄主植物往往不能提供足够的氮素[1],因此需要成虫来补充盐分或氮素[6]。另外,鳞翅目昆虫的趋泥行为仅发生在成虫阶段,除可能与成虫阶段所特有的一些行为有关,例如迁徙和繁殖等,也可能是因为在幼虫阶段移动缓慢且活动范围较小,搜寻及定位泥源困难,或在趋泥过程中若遇到天敌等不利因素时无法快速逃逸(因此幼虫阶段不会发生趋泥行为)。我们在研究黄脊竹蝗趋尿行为中发现,除成虫外,少量黄脊竹蝗5龄若虫也能发生趋尿行为[7],这是否是直翅目昆虫(渐变态昆虫)特有的现象需进一步研究。

  • 迄今为止,大量实例表明趋泥行为是一种典型的雄虫行为,主要是年轻的雄性蝶、蛾类成虫发生趋泥行为,雌性很少发生[6, 12-17, 32]。对此现象有学者提出了两种假说加以解释。

  • 绝大多数鳞翅目昆虫仅雄性成虫发生趋泥行。Alder统计了4年内发生趋泥行为的93种3 417个蛾类昆虫个体,雌性个体仅占1.3%[20];Beck等在婆罗洲岛观测到54种761头发生趋泥行为的蝴蝶全部为雄性个体,无一雌性[6]。对此现象学者提出了“婚姻馈赠假说(nuptial gift giving)”,推论雄虫通过趋泥行为从泥源中摄取营养物质并储存于精囊之中,在随后的交配过程中将精囊转移给雌虫,以此来转移除精子外的各种营养物质[33],以满足后者繁育的需要,从而获得精子竞争的胜利。这些馈赠的“礼物”可能含有多种矿物质,如钠盐[4-5, 34],钙等,也可能含有有毒的植物次生代谢产物[35-36],或者提供营养,比如氨基酸[29, 37]。同时,雄虫发生趋泥行为也降低了雌虫因暴露取食而被鸟类等天敌捕食或病菌感染的风险[4-5, 8, 13, 38]

  • 少数报道表明并非所有发生趋泥行为的鳞翅目昆虫均为雄性成虫,Downes等发现两种嗜食动物眼泪的夜蛾Arcyophora sylvaticaLobocraspis griseifusa雌、雄成虫均可发生趋泥行为,且雌、雄虫数量相当[39]。学者认为发生趋泥行为的昆虫性别与发育阶段有关,在成虫期的前、中期为雄性趋泥,而后期少量雌虫也会趋泥,这可能是由于成虫迁飞、生殖等特定行为造成的[13, 32]。咀嚼式口器昆虫黄脊竹蝗的趋泥行为与已报道的蝶、蛾类昆虫的趋泥行为存在明显差异,黄脊竹蝗5龄若虫和成虫均可发生趋泥行为,但成虫期仅雌虫发生趋泥行为(雌虫比例为99.77%)[7, 10, 22]。口器的不同是否是造成两类昆虫趋泥行为显著差异的原因还需试验数据证实。

3.   趋泥行为的驱动力机制
  • “趋泥”行为是昆虫适应环境、实现种群成功繁衍的一种特殊行为,涉及到行为、生理、生态及进化等多方面的内容,其激发机制相对复杂。尽管如此,近年来基于对碧凤蝶(Papilio bianor)、玉带凤蝶(Papilio polytes)及黄褐螯蛱蝶(Charaxes fulvescens)等典型昆虫趋泥行为的研究,Beck,Boggs及Molleman等国外学者先后提出了3种假说:

  • 水是所有陆生昆虫生长繁育过程中最为关键的物质之一,在干燥条件下,一些陆生昆虫因其相对较大的体表面积面临着大量失水的威胁,需要从外界摄取水以维持身体内的水分平衡[40]。大量关于的蝶、蛾类昆虫的趋泥行为的报道来自于乌干达等干旱地区或发生在炎热夏季[30, 32],而“泥源”(浅水、湿泥沙、粪便和尸体腐烂液等)中水含量丰富,因此有学者推测补充水可能是引起昆虫趋泥的重要原因[20-21]。仅在干旱的年份才发生趋泥行为的沙加缅都山脉格纹蛱蝶(Euphydryas editha bayensis)及吸食露水而导致体内水分含量明显升高的黑脉金斑蝶(Danaus plexippus)为此假说提供了证据[41]。另外,Launer等发现蓝蛱蝶(Phaedusa bensoni)在土耳其干旱炎热的草原上常大量聚集于浅水坑处吸水,而其在湿润的欧洲中部地区不发生趋泥行为[30]。研究还发现,发生趋泥行为的黑脉金斑蝶(Danaus plexippus)雄虫体内水分含量较未发生趋泥行为个体高6.7%[41]。另外,舒金平等及Yu等对黄脊竹蝗趋泥行为的研究表明,高温条件下竹蝗成虫对水分有强烈需求,在干滤纸和湿滤纸间显著偏好于湿滤纸[10, 40, 42]。但大量发生趋泥行为的鳞翅目昆虫会将多余水分排出体外,出现“蝴蝶排尿”的现象,这说明昆虫趋泥可能是摄取溶解在水里的物质而非水分[4-6]

    我们的研究表明黄脊竹蝗的趋泥行为与补充水分密切相关,竹蝗体内含水率较高的阶段,趋泥行为发生较弱,而随着虫体水分的丧失,成虫对水分的需求加大,发生趋泥行为的竹蝗数量显著增加[42],但水在昆虫趋泥行为中所发挥的具体作用需要更多的例证和试验数据加以阐释。

  • 昆虫是典型的变温动物,在一定范围内昆虫可通过特定的方式来调节身体温度以应对当环境温度变化对自身生长发育的不利影响[42-43]。统计表明,发生趋泥行为的昆虫主要集中在热带地区和炎热夏季的亚热带及温带地区,因此推测昆虫趋泥可能是为了降低自身体温以适应环境需要。多数研究表明,昆虫发生趋泥行为主要集中在热带地区和炎热夏季的温带地区,因此推测昆虫趋泥可能是为了降低自身体温[6-7, 15]。Frey等发现雄性黑脉金斑蝶会从加州中部海岸聚集点迁飞去临近的草地中吸食露水,吸食露水的雄蝶体表温度均低于未发生趋泥行为的雄蝶[41]。另外,笔者的研究结果也表明黄脊竹蝗的趋泥行为与环境温、湿度密切相关,“泥源”的诱蝗量与环境温度呈显著正相关(数据尚未发表)。但趋泥行为是为了降低自身温度这一推论目前还没有趋泥前后昆虫体温变化的直接试验数据支撑。

  • 通常“泥源”包括潮湿的泥沙、粪便(来自食肉性的脊椎动物或鸟类)、腐肉、海水、汗水、及动物眼泪等,泥源中往往富含盐类、氮素或氨基酸。一些学者在寻找关键性物质时发现,钠盐是泥源中的共性物质[4, 6, 8, 29, 44],而含氮化合物也是激发趋泥行为的关键物质[6-7, 45]

    盐分是表征陆生生物演化的关键物质,对植食性昆虫的发育和繁衍至关重要,但陆生植物叶片、茎干等植物组织中盐分含量较低,植食性昆虫仅通过幼虫阶段的取食往往无法满足成虫期生殖的需求而面临盐缺乏的问题[46-47],因而需要成虫通过趋泥行为从含盐浓度较高的泥源中摄食盐分,大量的研究结果也证实摄取钠盐是昆虫发生趋泥行为的主要原因[4-6, 29]。如,Arms发现在水、在Ca2+溶液及Na+溶液间东方虎凤蝶(Papilio glaucus)雄虫显著趋向于Na+溶液,浓度为10-3 M的钠盐溶液便可激发其趋泥行为[29];伊萨卡岛上的颤杨(Populus tremuloides)叶片钠盐含量为2.9 mg·g-1,明显低于当地其他树木的平均值,以颤杨为寄主的寡食性害虫Gluphisia septentrionis成虫嗜食钠盐溶液,发生趋泥行为的G.septentrionis雄虫体内Na+含量显著高于未发生该行为的雄虫,交配时雄虫将自身近50%钠盐(约10 pg)传递给雌虫,最终传入下一代[4-5]

    除此之外,由于腐肉、粪便等“泥源”可能富含蛋白质和氨基酸等资源,通过趋泥行为获取蛋白质,氨基酸,或铵盐也得到了试验证实[29, 48-49]。Beck用清蛋白、氨基酸、尿素及氯化钠等物质作为泥源引诱蝴蝶,结果表明氯化钠、清蛋白及氨基酸均可诱到蝴蝶成虫,其中以清蛋白的诱集量最大[6]。另外,我们研究表明黄脊竹蝗成虫对碳酸氢铵溶液及富含铵盐的发酵尿液有明显的取食偏好,在林间碳酸氢铵及发酵人尿的的诱蝗量显著高于氯化钠等盐溶液的诱蝗量[7, 10, 40, 49],可见氮素在昆虫趋泥行为中有重要的意义。

4.   趋泥行为对昆虫生理的影响
  • 钠盐如何作用于昆虫的消化、排泄、以及肌肉神经系统已经研究的很详尽[50-51],但鲜有研究指出补充摄取的钠盐如何影响昆虫的行为,Arms等提出昆虫肌肉神经系统需要大量钠盐,因此需要有较好飞行能力的昆虫(如蝴蝶中雄性成虫)发生趋泥现象[29]。Hall和Willmott发现有趋泥行为的蚬蝶科(Riodinidae)昆虫躯干粗壮而翅膀较小,飞行肌发达,飞行能力强[15],但在乌干达对斑豹蛱蝶(Speyeria mormonia)趋泥行为的研究未能证实这一点[12]。趋泥行为是典型的雄虫行为,因此在趋泥行为中摄取钠盐可能有提高精子活性,或有助于消化系统吸收更多的氨基化合物以促进昆虫生长和发育[52]

    研究表明,植食性昆虫摄取钠盐对繁殖有积极的作用,用经钠盐处理过的叶子来喂养蚜虫,蚜虫数量扩增速度加快[53]。雄虫通过精囊在交配中将获取钠盐提供给雌虫,雌虫再转移给卵,从而提升繁殖成功率[5, 34, 54]。最佳的例证是埃塞克斯弄蝶(Thymelicus lineola),幼虫孵化时,如果卵里的钠盐含量较高,则幼虫存活几率较高[34]。但是,对斑豹蛱蝶(Argynnis hyperbius)的研究发现,雄虫摄取钠盐的量对雌虫的产卵量及生殖能力没有积极影响[12]。可见,趋泥行为获取盐分对昆虫生殖生理的影响仍需试验验证[8]

  • 一般认为幼虫获取的氮素并转移到成虫阶段主要用于产卵和体壁的维护[55-57],雌虫阶段所获取氮素有助于其生殖力和卵孵化率的提高[58-59]。热带蟑螂(Xestoblatta hamata)雄虫对富含尿酸的鸟粪或者爬行动物的粪便有明显的偏好,随后将取食获得的尿酸盐通过交配传递给雌虫,这些尿酸盐能极大地提高雌虫的繁殖能力[60-61]。Arms等发现东方虎凤蝶(Papilio glaucus)雄虫通过趋泥行为摄取氨基酸,这些氮素最终会出现在与之交配的雌虫所产的卵中[29]。相反,Molleman和Midgley利用同位素示踪法来追踪氮素在Charaxes fulvescensC. bipunctatusC. numenes等5种发生趋泥行为的蛱蝶间的传递过程,结果发现在精囊及卵中均未发现标记氮素的存在[62]。另外,有研究者认为含氮化合物可能被用做营养物质或者飞行肌肉生长,从而提高这些种类的竞争力[63-64]。笔者在研究黄脊竹蝗趋泥行为发现,成虫产卵前,仅黄脊竹蝗雌虫趋尿,这可能与雌虫在交配中需要背负雄虫飞行迁移,寻找产卵地等行为有关,但从尿液中摄取的氮素是否用于繁殖或神经肌肉活动尚未明确[49]

5.   泥源的搜寻机制
  • 在自然界中,昆虫通过物理的或化学或二者结合的信号刺激来搜索定位寄主或产卵场所,如植食性昆虫主要通过植物挥发物指纹图谱来搜寻寄主植物[1],而昆虫在趋泥过程中如何定位到“泥”源尚未有明确的结论,开展的研究也相对较少。迄今,对于国内外学者提出了(1)视觉判断(昆虫依据泥源周围物体或昆虫的颜色、形态等可视要素来判定“泥”源的位置)[6, 65](2)嗅觉定位(昆虫依据泥源所释放的挥发性气味来定位“泥”源)[7](3)听觉定向(昆虫依据同伴聚集或取食时发出的声音信号来定位“泥”源)[65]3种解释来推测昆虫搜寻及定位泥源的方法,但都缺乏有说服力的试验证据[8]。Inoue等通过超微解剖和电生理试验证实碧凤蝶(Papilio bianor)和蓝凤蝶(Papilio protenor)雄成虫喙内有大量的味觉感器,并通过这些味觉感器来探知环境中的Na+浓度以定位泥源,探知的钠盐浓度范围在1 mM to 1 M之间[66];Otis等利用蝴蝶模型证实了社会助长效应(social facilitation)在Battus philenorPapilio glaucus两种蝴蝶的趋泥行为中起关键作用,成虫对摆放的蝴蝶模型有明显的趋向[65];Beck也发现类似现象,一些粉蝶能被同等大小、性状类似的蝴蝶模拟物诱集[6];Yu等通过黄脊竹蝗成虫在不同颜色的选择性试验推测颜色在黄脊竹蝗趋泥行为中可能发挥重要作用,结果表明在经NaCl溶液处理的黄色、绿色和白色滤纸之间,黄脊竹蝗成虫显著偏好于绿色滤纸[67];舒金平等的EAG测定、挥发物行为生测及林间诱杀等结果证实人尿挥发物在黄脊竹蝗定位“泥源”的过程中发挥着重要作用[11]。对于蟑螂等一些群集性昆虫,雄虫发现泥源后的敲击声可能是同类定位的主要依靠[68]。昆虫的趋泥行为是一个复杂的生理生化过程,其搜寻泥源过程可能是多个因素共同作用的结果。

6.   趋泥行为在害虫防治中应用
  • 发生趋泥行为的昆虫对泥源有显著的趋向,可用于鳞翅目成虫的诱集[48, 65]。程佳及Yu等利用钠盐和铵盐进行了林间黄脊竹蝗诱杀,效果显著[22, 69],是首例报道的利用昆虫趋泥行为进行重要害虫防治的案例。我们系统筛选了可用于黄脊竹蝗诱杀的“泥源”配方,并通过连续5d的成虫诱杀,林间黄脊竹蝗的虫口密度由原来的11.9头·诱捕器-1下降至2.6头·诱捕器-1,差异显著[70]

7.   展望
  • 趋泥行为在植食性的节肢动物中是一种常见的自然现象,近20年来,有关“什么样的昆虫要趋泥?” “昆虫为何趋泥?” “趋泥行为的生态学意义是什么?”等一系列核心科学问题的探索受到广泛关注。然而,对昆虫趋泥行为的研究报道虽多,但迄今为止,对于上述关键问题的回答是争论多于结论。虽然诸多研究表明钠盐和氮素是引发趋泥行为最为关键的因素,但是却并不能排除或者证明泥源中其他物质的作用。同时先前的研究极少涉及“激发昆虫的趋泥行为的钠盐或氮素的浓度阈值,虽然方蓉等及Inoue等对昆虫趋泥行为的发生与钠盐或氮素浓度的关系进行了探讨,但仍未揭示激发该行为的浓度阈值[49, 66]。当前趋尿行为的主要研究对象集中在蝶蛾类吸收式口器昆虫,缺少与咀嚼式口器昆虫等不同类型昆虫趋泥行为的对比研究,而基于典型的不同类型昆虫趋泥行为间的对比研究,往往可明显加深对这一特殊行为生态学及进化学意义的发掘和理解。

    另外,重点研究趋泥行为是否或者如何影响昆虫生理生化活动可能更易深入了解趋泥行为的生物学意义。趋泥行为对昆虫生理生化的影响可能存在于多个方面,例如提高昆虫神经肌肉的反应能力、飞行能力、生殖力及孵化率等[71-72]。但是目前的研究并未给出究竟除食物外补充摄取多少盐分或氮素会对昆虫的生理产生积极影响,所提出的“趋泥行为能够提高神经肌肉反应能力的假说”也没有可靠的试验数据来证明。另外,趋泥行为在昆虫行为生态学及进化生物学上的作用也同样至关重要,为此,为了更好更全面的理解昆虫的趋泥行为,就需要整合更多层面上的研究。

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