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普通大蓟马（Megalurothrips usitatus）是一种植食性蓟马，主要以热带和亚热带豆科植物为食，目前该虫已广泛分布于亚洲、大洋洲和美洲的一些国家或地区[1−2]。在我国海南省，该虫已成为豇豆（Vigna unguiculata）种植中的重要有害生物，其成虫和若虫均以豇豆嫩叶、花朵和豆荚为食，对作物造成严重危害，给豇豆的安全生产和增产增收带来了极大的困难和挑战[3−6]。作为单倍−二倍体（haplodiploidy）生物，普通大蓟马采用两性生殖和产雄孤雌生殖（arrhenotoky）繁衍后代[6]。性比和繁殖力在蓟马种群数量增长中起着非常关键的作用[7]，因此，探究普通大蓟马性比和繁殖力变化规律及影响因子，对绿色防控技术的探求具有重要意义。近年来的研究表明，同种雌性成虫释放的气味、作物施氮水平和紫外光是影响普通大蓟马性别分配的干扰因子[8−10]，而寄主植物、杀虫剂亚致死剂量、章鱼胺和酪胺，以及水杨酸甲酯气味则对子代性比无明显影响[6,11−13]。普通大蓟马繁殖力的重要影响因子包括食物[5,11,14−15]、繁殖方式[11]、种间竞争[16]、温度[3]、杀虫剂[6]、氮肥施用水平[9]等。
在蓟马防治实践中，环境友好的防控措施广受重视与应用[1,17]。植物挥发性有机化合物（VOCs）已成为蓟马研究领域中的热点[18−20]。多数研究侧重于评价挥发物对蓟马行为的影响及其毒杀活性，而有关挥发物对蓟马性比与繁殖力影响的研究则鲜有报道。香芹酚（又称香荆芥酚，carvacrol），是一种挥发性单萜酚，属于单萜类化合物，其化学名称为5-异丙基-2-甲基苯酚，是多种芳香植物精油的重要组分，具有广泛的生物活性，包括杀虫、抗菌等作用[21–22]。该挥发物对部分害虫展现出良好的熏杀和触杀效果[23−27]，其作用位点多样化[28–29]，涉及γ-氨基丁酸A型受体（GABAARs）[30]、烟碱型乙酰胆碱受体（nAChRs）[31]、章鱼胺受体（octopamine receptors）[32–33]、酪胺受体（tyramine receptors）[34]和乙酰胆碱酯酶（AChE）[35–36]等位点。目前，香芹酚对蓟马的影响研究主要集中在几种植食性蓟马，其活性主要表现在对烟蓟马（Thrips tabaci）和西花蓟马（Frankliniella occidentalis）的产卵阻滞作用[18−19, 37–38]、对烟蓟马雌虫的驱避性[39]、对西花蓟马若虫的触杀活性[40–41]，以及对玉米黄呆蓟马（Anaphothrips obscurus）成虫和若虫的熏杀活性[42]。然而，有关香芹酚对普通大蓟马繁殖影响的研究仍属空白。本研究拟采用亲代雌虫熏蒸法，评价高、低2种浓度香芹酚气味对已交配普通大蓟马雌虫的繁殖和性别分配的影响，旨在为挥发物在蓟马有害生物综合治理（integrated pest management，IPM）中的应用提供理论依据。
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豇豆（品种：纯丰长豇豆Vigna unguiculata），种植于网室大棚内，按常规方法进行栽培管理。挑选健康的幼嫩豆荚作为普通大蓟马的食物。
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在海南大学海甸校区农科教学实验基地，采集豇豆花内的普通大蓟马成虫，在（26±1）℃、相对湿度（60±5）%、光周期L:D=14:10条件下，用幼嫩豇豆豆荚进行饲养。子代化蛹后，将蛹单头饲养于玻璃试管（12 mm ×100 mm）内。刚羽化的成虫按性比1:1进行配对饲养24 h。最后，挑选健康的、1日龄已交配雌虫作为试虫[6,8−9]。
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试验所需试剂包括Sigma公司出产的石蜡油和99%香芹酚。石蜡油用于配制不同浓度的香芹酚溶液[43]。
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参照Lu等[42]的报道结果，并根据前期预备试验结果，本研究设置3个处理，即对照组（CK，0 μL·L–1香芹酚）、0.05 μL·L–1香芹酚和0.1 μL·L–1香芹酚。试验方法参照曹冉等[13]的报道。具体步骤概述如下：将1段幼嫩豇豆豆荚放入离心管（5 mL，管侧有1个防逃逸透气孔）内，接入1头1日龄已交配雌虫后以棉球封住管口。然后，将离心管放置在特制试管架上，每架10支离心管，接着将试管架转移至玻璃密封罐（2 L）中。离心管（1.5 mL）内置滤纸条（5 mm × 10 mm），滴入0.2 mL不同浓度香芹酚溶液，用作香芹酚气味源。密封罐内空气被洁净空气完全置换后，放置香芹酚气味源，然后立即封罐，让密封罐内香芹酚气味浓度分别为0（不含香芹酚）、0.05和0.1 μL·L–1。每天更换离心管中的豆荚和香芹酚气味源，直到亲代雌虫死亡。每个处理设30次重复（即30头亲代雌虫）。将更换出来的豆荚转移到新的玻璃试管（12 mm × 100 mm）中继续饲养，直至子代成虫羽化。在此期间，所有处理的蓟马子代均不接触香芹酚气味。亲代雌虫及其子代的饲养条件设定为（26±1）℃、相对湿度（60±5）%、光周期L:D=14h:10h。每天观察和记录亲代雌虫的存活、初孵若虫的数量、以及子代成虫的性别和数量，计算子代性比（即雄性占成虫比例）和日性比，以及子代存活率（即成虫占初孵若虫百分比）。
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利用Excel 2019进行试验数据处理和绘图。利用SPSS v26.0软件进行试验数据的统计分析。性比和存活率数据经反正弦转换后进行方差分析和多重比较（Duncan多重比较法，P<0.05）。
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子代雄虫数量：对照组、0.05和0.1 μL·L–1香芹酚处理的普通大蓟马子代雄虫数平均值分别为110.03、133.33和50.30头·雌–1，其中，0.1 μL·L–1香芹酚处理与前2个处理之间均有显著差异（P＜0.05），但0.05 μL·L–1香芹酚处理与对照组差异不显著（图1）。
图 1 已交配普通大蓟马雌虫在香芹酚气味胁迫下所产子代成虫数量
Figure 1. Number of adult offsprings from Megalurothrips usitatus mated females under exposure to carvacrol odor
子代雌虫数量：0.1 μL·L–1香芹酚处理（92.57头·雌–1）显著小于对照组（138.50头·雌–1）和0.05 μL·L–1香芹酚（135.30头·雌–1）（P＜0.05），而0.05 μL·L–1香芹酚处理与对照组之间没有差异。
子代成虫数量：在考虑总体子代数量方面，0.1 μL·L–1香芹酚处理仅有142.87头·雌–1，与对照组（248.53头·雌–1）和0.05 μL·L–1香芹酚处理（268.63 头·雌–1）之间的差异都达到了显著水平（P＜0.05），但0.05 μL·L–1香芹酚处理与对照组没有显著差异。
由此可见，高浓度（0.1 μL·L–1）香芹酚气味确实能够影响已交配普通大蓟马雌虫的繁殖。
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已交配普通大蓟马雌虫在香芹酚熏蒸状态下一生所产子代的雄性比见图2。在0.05和0.1 μL·L–1香芹酚的处理下雄性比分别为0.46和0.35，两者之间差异显著（P＜0.05）。与对照（0.41）相比，0.05 μL·L–1香芹酚处理的雄性比提高了12.93%，而0.1 μL·L–1香芹酚处理的雄性比则下降了15.94%，但是，这两个浓度的香芹酚都没有显著改变普通大蓟马的性别分配。
图 2 已交配普通大蓟马雌虫在香芹酚气味胁迫下所产子代的性比
Figure 2. Sex ratio of offspring from Megalurothrips usitatus mated females under exposure to carvacrol odor
除了产卵第8~10天和第21~22天之外，在普通大蓟马产卵期的每一天，各处理的日性比之间都没有显著差异（图3）。0.1 μL·L–1香芹酚处理在产卵第8天和第10天的性比最小，同为0.14，均仅与0.05 μL·L–1香芹酚处理有显著差异（P＜0.05）。同样地，在产卵第9天，以0.1 μL·L–1香芹酚处理的性比最小，仅为0.18，与对照（0.29）和0.05 μL·L–1香芹酚处理（0.33）的差异都到达了显著水平（P＜0.05）。对照组在产卵第21天和22天的性比分别高达0.68和0.84，均显著大于其他两个香芹酚处理（P＜0.05）。
图 3 已交配普通大蓟马雌虫在香芹酚气味胁迫下所产子代性比日动态
Figure 3. Daily variation in offspring sex ratio in Megalurothrips usitatus mated females under exposure to carvacrol odor
香芹酚处理的性比日动态与对照基本相似。在亲代雌虫产卵期的前期，3个处理的日性比基本保持偏雌性。对照组、0.05和0.1 μL·L–1香芹酚处理的亲代雌虫产卵期分别进入产卵第20天、第25天和第22天后，子代日性比全部偏雄，且呈逐步上升趋势。在亲代雌虫产卵期的后期，所产子代全为雄性；对照组、0.05和0.1 μL·L–1香芹酚处理的全产雄阶段（即性比等于1.0）的开始时间分别出现于产卵第36天、第42天和第36天。总体上，和对照组相比，低浓度和高浓度香芹酚处理实际均不改变普通大蓟马产卵期间的性比变化，均呈现前24天或21天偏雌、后期偏雄的特点。
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经香芹酚熏蒸处理的已交配普通大蓟马雌虫所产子代的存活率见图4。对照组、0.05和0.1 μL·L–1香芹酚处理的子代存活率分别为94.42%、90.65%和83.31%，彼此之间都有显著差异（P＜0.05）。用0.05和0.1 μL·L–1香芹酚处理的子代存活率分别比对照组降低了4.00%和11.77%。
图 4 已交配普通大蓟马雌虫在香芹酚气味胁迫下所产子代的存活率
Figure 4. Survival rate of offspring from Megalurothrips usitatus mated females under exposure to carvacrol odor
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0.05 μL·L–1香芹酚处理能显著延长普通大蓟马亲代雌虫的产卵期，时长可达36.63 d，与对照组（28.60 d）和0.1 μL·L–1香芹酚处理（26.17 d）差异显著（P＜0.05）（表1）。但是，香芹酚气味胁迫对普通大蓟马雌虫产卵后期没有显著影响，3个处理的产卵后期介于0.70～ 1.27 d。用0.05 μL·L–1香芹酚熏蒸处理的普通大蓟马雌虫存活更久，时长为37.90 d，显著大于对照组（29.67 d）和0.1 μL·L–1香芹酚处理（26.87 d）（P＜0.05）。总体上，和对照组相比，低浓度（0.05 μL·L–1）的香芹酚能显著延长产卵期、高浓度（0.1 μL·L–1）则不能，2个浓度的香芹酚对产卵后期均无影响。
表 1 已交配普通大蓟马雌虫在香芹酚气味胁迫下的发育历期
Table 1. Development time of Megalurothrips usitatus mated females under exposure to carvacrol odor
处理 Treatments 发育历期 Development time/d 产卵期 Oviposition period 产卵后期 Post-oviposition period 存活时间 Surviving time CK 28.60±1.36b 1.07±0.19a 29.67±1.38b 0.05 μL·L–1香芹酚 Carvacrol 36.63±1.18a 1.27±0.30a 37.90±1.11a 0.1 μL·L–1香芹酚 Carvacrol 26.17±1.26b 0.70±0.27a 26.87±1.24b 注：表中数值为平均数±标准误。同列数据后不同字母表示在P<0.05差异显著（Duncan多重比较法）。
Note: Data are mean±SE, and followed by different letters within the same column are significantly different at 0.05 level by Duncan’s multiple range test. -
用亚致死浓度为0.05和0.1 μL·L–1的香芹酚熏蒸处理普通大蓟马雌虫对其繁殖有干扰作用。高浓度（0.1 μL·L–1）香芹酚气味能降低普通大蓟马所产子代的成虫数，但是低浓度（0.05 μL·L–1）香芹酚则无影响。低浓度和高浓度香芹酚能使子代存活率分别降低4.00%和11.77%。低浓度香芹酚熏蒸还能延长亲代雌虫的产卵期和存活时间，但高浓度香芹酚则对产卵期无显著影响。
两种浓度香芹酚熏蒸对普通大蓟马产后代能力的影响符合常见的双相剂量-效应（biphasic dose-response）模式，即低剂量起刺激作用或无作用，高剂量则表现为抑制作用[44]。香芹酚熏蒸引发的繁殖抑制效应也出现于其他昆虫，如黑腹果蝇（Drosophila melanogaster）[45]、菜豆象（Acanthoscelides obtectus）[46]、四纹豆象（Callosobruchus maculatus）[47–48]等。同样地，香芹酚对菜豆象和四纹豆象繁殖力的抑制作用随香芹酚熏蒸浓度的增加而增强[46−48]。此外，非熏蒸法试验证实，某些杀虫剂亚致死剂量对其他蓟马繁殖力的影响也展现出了类似的剂量-效应，例如，残膜法处理西花蓟马2龄若虫[49]、叶片喷施残留法处理柑橘蓟马（Scirtothrips citri）成虫[50]等。在Sedy等[37]和Allsopp等[38]的研究中，采用喷施残留法处理蓟马雌虫，结果发现，高浓度香芹酚对烟蓟马[37]和西花蓟马[37–38]产卵的抑制作用更加明显，他们所评价的是香芹酚的触杀或胃毒活性对这两种蓟马产卵的阻滞效应。本研究采用的是亲代雌虫熏蒸法，所评价的是香芹酚气味对普通大蓟马繁殖力的直接影响。
香芹酚熏蒸对普通大蓟马雌虫的产卵期和存活时间展现出了低剂量兴奋效应（hormesis）。这是昆虫对香芹酚低剂量兴奋效应的首次报道。Lazarević等[51]曾发现，0.5%百里香精油能显著延长菜豆象雌虫的存活时间。百里香酚（thymol）与香芹酚互为异构体[52]，是百里香精油的主要活性组分[51]。低剂量兴奋效应的呈现可能跟昆虫体内抗氧化酶和解毒酶活性的增强有关，涉及超氧化物歧化酶（SOD）、过氧化氢酶（CAT）、谷胱甘肽S移换酶（GST）等关键酶[44,52−54]。
综上所述，以浓度为0.05和0.1 μL·L–1的香芹酚熏蒸处理已交配普通大蓟马雌虫对3个繁殖参数的影响呈现出了不一样的剂量效应。香芹酚气味对繁殖力的影响呈现“低剂量无作用、高剂量抑制作用”；对亲代雌虫的产卵期和存活时间则表现为“低剂量刺激作用、高剂量无作用”；对子代存活率的影响体现出“低剂量和高剂量同为抑制作用”。这种差异反应了普通大蓟马不同繁殖参数对香芹酚浓度的敏感性有所不同。因此，为了全面评价某种挥发物对蓟马的影响，应充分考虑挥发物亚致死浓度所起的作用。
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用浓度为0.05 μL·L–1和0.1 μL·L–1的香芹酚熏蒸处理普通大蓟马雌虫，对子代性比没有明显影响。尽管高浓度（0.1 μL·L–1）香芹酚能降低其繁殖力，但子代雄虫和雌虫的发育均受到抑制，因而子代性比没有显著变化。香芹酚气味对普通大蓟马性别分配的无干扰效应很可能与香芹酚杀虫机理的多样化有关。香芹酚的作用位点包括γ-氨基丁酸A型受体、烟碱型乙酰胆碱受体、章鱼胺受体、酪胺受体和乙酰胆碱酯酶等[28−36]。在熏蒸过程中，香芹酚通过昆虫的呼吸系统进入虫体内，其具体作用机制是通过一种或几种位点来实现的？不同作用位点之间是否存在协同或拮抗作用呢？这两个问题有待进一步研究。目前可以确定的是，章鱼胺受体和酪胺受体很可能不参与普通大蓟马性别分配，大量的实验结果表明：饲喂章鱼胺和酪胺的普通大蓟马雌虫对其子代性比没有显著影响[12]；双甲脒亚致死剂量[6]和水杨酸甲酯气味[13]都不能显著改变该虫的性比，而双甲脒和水杨酸甲酯的作用位点跟章鱼胺受体有关。此外，杀虫剂亚致死剂量干扰子代性比的案例也出现在寄生蜂中，它们繁殖方式相似且同属单倍二倍体生物。Delpuech和Meyet[55]的研究发现，毒死蜱（氯吡硫磷）LD20（即20%致死剂量）处理甘蓝夜蛾赤眼蜂（Trichogramma brassicae）雌蜂能导致子代的雌性比变小。Costa等[56]采用硫双威和氟吡呋喃酮间接处理寄主体内的短管赤眼蜂（Trichogramma pretiosum）非成虫个体后，F0代的子代雌性比显著下降，硫双威还能进一步压低F1代的雌性比。毒死蜱和硫双威是乙酰胆碱酯酶抑制剂，而氟吡呋喃酮则是作用于昆虫乙酰胆碱受体的杀虫剂，这三种化合物的杀虫机制各不相同，但均涉及昆虫神经系统。因此，有必要进一步探讨乙酰胆碱酯酶和乙酰胆碱受体是否参与了普通大蓟马的性比调节。这一问题值得深入研究，基于此，未来的研究应选择具有不同杀虫机理的挥发物或杀虫剂，用亚致死剂量处理普通大蓟马，从而系统的揭示普通大蓟马性别分配的内在机理，探索影响子代性比的关键因素，最终为实现子代性比高度偏雄、提升绿色防控效果提供科学依据。
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本研究采用亲代雌虫熏蒸法，评价了高低2个浓度香芹酚气味对已交配普通大蓟马雌虫的繁殖力和性比的影响。结果显示，高浓度（0.1 μL·L–1）香芹酚气味能显著降低普通大蓟马所产子代的雄虫数、雌虫数和成虫数，但是低浓度（0.05 μL·L–1）香芹酚则无影响。低浓度和高浓度香芹酚处理均没有显著改变其子代性比，且子代性比日动态也与对照基本相似。低浓度和高浓度香芹酚能够分别显著降低子代存活率4.00%和11.77%。此外，低浓度香芹酚熏蒸还能显著延长亲代雌虫的产卵期和存活时间，但高浓度香芹酚则对产卵期无显著影响。此外，2个浓度香芹酚对产卵后期均无显著影响。由此可见，以浓度为0.05和0.1 μL·L–1的香芹酚熏蒸处理已交配普通大蓟马雌虫对性别分配没有明显影响，但高浓度香芹酚促使其繁殖能力下降。此结果可为普通大蓟马绿色防控新对策的研发提供数据支撑。
香芹酚熏蒸处理亲代雌虫对普通大蓟马繁殖的影响
DOI: 10.15886/j.cnki.rdswxb.20250105
CSTR: 32425.14.j.cnki.rdswxb.20250105
Impact of maternal exposure to carvacrol fumigation on reproduction of Megalurothrips usitatus (Bagnall) (Thysanoptera: Thripidae)
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摘要: 香芹酚（Carvacrol）是一种具有杀虫活性的挥发性单萜酚。为了探明香芹酚气味对普通大蓟马（Megalurothrips usitatus）繁殖和性比的潜在影响，采用不同浓度[0（CK）、0.05和0.1 μL·L–1]的香芹酚对已交配的1日龄雌虫进行终身熏蒸，每天以幼嫩豇豆（Vigna unguiculata）豆荚供其取食和产卵。所产下的子代在没有香芹酚气味条件下继续饲养至成虫羽化。结果显示，仅在高浓度香芹酚（0.1 μL·L–1）处理下，雌虫一生所产雄性和雌性子代的数量显著减少，分别比对照减少54.29%和33.16%（P＜0.05）；在低浓度（0.05 μL·L–1）和高浓度的香芹酚处理下雄性比分别为0.46和0.35，与对照之间的差异均不显著。经对照组、低浓度和高浓度香芹酚处理的子代存活率分别为94.42%、90.65%和83.31%，彼此之间差异显著（P＜0.05）。低浓度香芹酚还显著延长亲代雌虫的产卵期和存活时间。本研究结果表明，香芹酚熏蒸处理已交配的普通大蓟马雌虫对其性别分配没有明显影响，但高浓度香芹酚会抑制其繁殖能力。Abstract: Carvacrol is a volatile phenolic monoterpene with insecticidal activities. One-day-old mated females of Megalurothrips usitatus were fumigated until death with carvacrol at concentrations of 0 (CK), 0.05, and 0.1 μL·L–1 air, respectively in an attempt to investigate potential effect of carvacrol odor on reproduction and sex ratio of M. usitatus,. Young cowpea pods were daily provided as their feeding and oviposition sites. The offspring produced by the treated females were reared without carvacrol odor exposure until adult eclosion. The results exhibited that the number of adult male offspring and adult female offspring from the females treated with carvacrol only at 0.1 μL·L–1 was significantly reduced by up to 54.29% and 33.16% compared with those of the control, respectively. The sex ratio (proportion male) of the offspring produced by the females exposed to 0.05 and 0.1 μL·L–1 of carvacrol was 0.46 and 0.35, respectively, both of which did not significantly differ from that of the control. The survival rate of the offspring for the control and carvacrol treatments at the concentrations 0.05 and 0.1 μL·L–1 was 94.42%, 90.65%, and 83.31%, respectively, being significantly different from each other. Furthermore, both oviposition duration and surviving time of the focal females under the exposure to 0.05 μL·L–1 of carvacrol were significantly prolonged. This study reveals that carvacrol fumigation does not play a role in sex allocation in mated females of M. usitatus, but exerts high-dose inhibition to their offspring production.
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Key words:
- Megalurothrips usitatus /
- Vigna unguiculata /
- carvacrol /
- reproduction /
- sex ratio
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图 2 已交配普通大蓟马雌虫在香芹酚气味胁迫下所产子代的性比
注：图中数据为平均值±标准误。柱上标有不同字母时，表示在P<0.05上差异显著（Duncan多重比较法）。下图同。
Fig. 2 Sex ratio of offspring from Megalurothrips usitatus mated females under exposure to carvacrol odor
Note: Data are mean ± SE. Bars with different letters indicate significant difference at 0.05 level by Duncan’s multiple range test. Similarly hereinafter.
图 3 已交配普通大蓟马雌虫在香芹酚气味胁迫下所产子代性比日动态
注：图中数据为平均值±标准误。同一天数据标记上标有不同字母时，表示在P<0.05上差异显著（Duncan多重比较法）。
Fig. 3 Daily variation in offspring sex ratio in Megalurothrips usitatus mated females under exposure to carvacrol odor
Note: Data are mean ± SE. Data marker with different letters on the same oviposition day indicates significant difference at 0.05 level by Duncan’s multiple range test.
图 4 已交配普通大蓟马雌虫在香芹酚气味胁迫下所产子代的存活率
Fig. 4 Survival rate of offspring from Megalurothrips usitatus mated females under exposure to carvacrol odor
表 1 已交配普通大蓟马雌虫在香芹酚气味胁迫下的发育历期
Table 1 Development time of Megalurothrips usitatus mated females under exposure to carvacrol odor
处理 Treatments 发育历期 Development time/d 产卵期 Oviposition period 产卵后期 Post-oviposition period 存活时间 Surviving time CK 28.60±1.36b 1.07±0.19a 29.67±1.38b 0.05 μL·L–1香芹酚 Carvacrol 36.63±1.18a 1.27±0.30a 37.90±1.11a 0.1 μL·L–1香芹酚 Carvacrol 26.17±1.26b 0.70±0.27a 26.87±1.24b 注：表中数值为平均数±标准误。同列数据后不同字母表示在P<0.05差异显著（Duncan多重比较法）。
Note: Data are mean±SE, and followed by different letters within the same column are significantly different at 0.05 level by Duncan’s multiple range test.
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