桑天牛卵啮小蜂识别已寄生刻槽的化学机制
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摘要
桑天牛(Apriona germari Hope)是我国重要的蛀干害虫,桑天牛卵啮小蜂(Aprostocetus prolixus)是桑天牛重要的卵期寄生性天敌。本文对该寄生蜂识别已寄生桑天牛刻槽的化学机制进行了研究,这对于揭示桑天牛卵啮小蜂的寄生机制,以及利用该寄生蜂控制桑天牛危害具有重要意义。
在正常刻槽与某种已寄生刻槽(它蜂寄生或自己寄生的刻槽)同时存在的条件下,雌蜂首先接触到正常刻槽的次数明显高于已寄生刻槽(正常-它蜂寄生:P < 0.01,正常-自己寄生:P < 0.001),找到正常刻槽的时间明显少于已寄生刻槽(正常-它蜂寄生:P < 0.001,正常-自己寄生:P = 0.008),这表明桑天牛卵啮小蜂在寄生过程中的某个(或某些)环节对刻槽进行了标记,而这种标记物在近距离内被桑天牛卵啮小蜂感知,并对该寄生蜂产生趋避作用,使其优先选择正常刻槽;寄生蜂在正常刻槽上的搜索时间、刺探时间和寄生率也都明显高于已寄生刻槽(搜索时间:正常-它蜂寄生P = 0.002,正常-自己寄生P = 0.006;刺探时间:正常-它蜂寄生P = 0.006,正常-自己寄生P = 0.008;寄生率:正常-它蜂寄生P < 0.01,正常-自己寄生P < 0.001)。说明在正常刻槽和某种已寄生刻槽同时存在时,桑天牛卵啮小蜂优先寄生正常刻槽,避免过寄生。
当它蜂寄生和自己寄生刻槽都存在时,桑天牛卵啮小蜂对这两种已寄生刻槽的行为参数间没有显著性差异(接触到两种刻槽的次数:P > 0.05;找到刻槽所需时间:P = 0.499;搜索时间:P = 0.612;刺探时间:P = 0.310;寄生率:P > 0.05),这表明桑天牛卵啮小蜂不具有区分它蜂寄生刻槽和自己寄生刻槽的能力。
在非选择实验中,与已寄生刻槽(它蜂或自己寄生刻槽)相比,卵啮小蜂更易于在正常刻槽上产卵寄生(正常-它蜂:P = 0.024;正常-自己:P = 0.010),这再次证明了桑天牛卵啮小蜂在寄生过程中对刻槽进行了标记。当雌蜂只能面对某种已寄生刻槽时,其过寄生率为56%;而在有正常刻槽可供选择的情况下,已被寄生刻槽的寄生率为14.3%,这表明在没有正常刻槽存在时,卵啮小蜂也会利用已被寄生的刻槽。
通过选择实验发现,卵啮小蜂对正常刻槽和有爬行痕迹刻槽的行为参数间无显著差异(正常刻槽-有它蜂爬行痕迹刻槽:刻槽首先被接触到的次数,P > 0.05;找到每种刻槽所需时间,P = 0.476;搜索时间,P = 0.931;刺探时间,P = 0.420;寄生率,P > 0.05;正常刻槽-有自己爬行痕迹刻槽:刻槽首先被接触到的次数,P > 0.05;找到每种刻槽所需时间,P = 0.931;搜索时间,P = 0.678;刺探时间,P = 0.859;寄生率,P > 0.05)。这表明卵啮小蜂不能区分正常刻槽和被自己或其他个体搜索过的刻槽,说明卵啮小蜂在搜索过程中(包括触角搜索和产卵器刺探行为)没有标记刻槽。
当桑天牛卵啮小蜂同时面对正常刻槽和已被寄生但未被寄生蜂产卵器涂抹的刻槽时,每种刻槽首先被寄生蜂接触到的次数没有明显差别(P > 0.05),寄生蜂接触到每种刻槽所需要的时间也无显著差异(P = 0.638),在两种刻槽上的搜索时间、刺探时间以及寄生率等方面均无明显差异(搜索时间,P = 0.538;刺探时间,P = 0.433;寄生率,P > 0.05),说明卵啮小蜂不能识别正常刻槽和已被寄生但未被寄生蜂产卵器涂抹的刻槽。同时也表明,在寄生过程中,寄生蜂在刻槽表面搜索、刺探、产卵器对桑天牛卵检测、产卵均未对刻槽表面及刻槽内的桑天牛卵进行标记。
综合以上实验结果不难发现,只有被桑天牛卵啮小蜂产卵器涂抹后的刻槽上具有产卵标记,这种涂抹行为不会对刻槽表面产生物理标记,只能是化学标记,即标记信息素。
通过非选择实验发现,桑天牛卵啮小蜂在正常刻槽上的寄生率明显高于被寄生一次或寄生两次的刻槽(正常-它蜂寄生一次:P = 0.028;正常-它蜂寄生两次:P = 0.000),在被寄生一次刻槽上的寄生率明显高于寄生两次的刻槽(P = 0.013)。这表明随着刻槽被寄生次数的增多,在刻槽表面累积的标记信息素也增多。
对桑天牛卵啮小蜂雌蜂头、胸、腹部提取物的生测实验中,首次接触到滴加二氯甲烷的小蜂腹部提取物的刻槽的次数明显少于对照刻槽(只滴加二氯甲烷溶剂的正常刻槽)(P < 0.05),在滴加二氯甲烷的小蜂腹部提取物的刻槽上的搜索时间明显少于对照刻槽(P < 0.05) ,而滴加其他溶剂提取物的刻槽与对照相比则无显著差异,表明该寄生蜂标记信息素来源于寄生蜂腹部,且二氯甲烷为提取该寄生蜂标记素的最佳溶剂。
GC-MS(气相色谱-质谱联用仪)结果表明,桑天牛卵啮小蜂腹部的二氯甲烷提取物包括烃类、醛类、脂肪酸、酯类和萜类等5类化合物。烃类物质有20种,含量为40.55%,;醛类物质有3种,含量为0.32%;含有7种脂肪酸,含量为54.96%;酯类化合物为2种,含量为3.7%,萜类物质两种,含量为0.18%。
在对桑天牛卵啮小蜂杜氏腺、毒囊毒腺、卵巢的二氯甲烷提取物的生物测定实验中,寄生蜂找到对照刻槽的时间明显少于滴加杜氏腺提取液的刻槽(P = 0.048),在对照刻槽上的搜索时间明显多于滴加杜氏腺提取液的刻槽(P = 0.039),在对照刻槽上的寄生率也高于滴加杜氏腺提取液的刻槽(P < 0.001)。而寄生蜂在滴加毒囊毒腺或卵巢提取物刻槽上的行为参数与对照刻槽相比没有显著差异,这表明杜氏腺的提取物对卵啮小蜂有趋避和抑制产卵的作用,说明桑天牛卵啮小蜂的标记信息素来源于杜氏腺。
通过选择实验发现,桑天牛卵啮小蜂在对照刻槽(滴加二氯甲烷溶剂)上的寄生率明显高于滴加10μg二十四烷的刻槽(P < 0.05),首次接触到对照刻槽的次数明显多于滴加10μg棕榈酸的刻槽(P < 0.05),而1μg的棕榈酸和1μg二十四烷、十六烷(1μg和10μg)和二十七烷(1μg和10μg)对卵啮小蜂的寄主识别行为没有影响,说明棕榈酸和二十四烷为卵啮小蜂的标记信息素的重要组分。
Aprostocetus prolixus is an important egg parasitoid of A. germari, stem borer infesting many species of trees. This paper investigated the chemical mechanism in discrimination of previously prarasitized hosts by the parasitoid, which is very important to reveal the mechanism of parasitization by A. prolixus and use the parasitoid to control A. germari.
When the healthy host and the host previously parasitized (conspecific-parasitized or self-parasitized) in the same pacth, the number of healthy host firstly contacted is significantly higher than the previously parasitized host (healthy host vs conspecific-parasitized, P < 0.01; healthy hosts vs self-parasitized, P < 0.001). The time for A. prolixus finding healthy host was much less than that for searching previously prarsitized host (healthy host vs conspecific-parasitized host, P < 0.001; healthy host vs self-parasitized host, P < 0.008). It was demonstrated that A. prolixus had marked the host in some stage of the process of parasitization.The markers can be perceived by the parasitoid in short distance and have repellent effect to herself or other individuals, which make the parasitoid prefer choosing the healthy host. The searching time, probing time and parasitization rate were significantly higher than previously parasitized hosts (searching time: healthy host vs conspecific-parasitized host, P = 0.002; healthy hosts vs self-parasitized host: P = 0.006. probing time: healthy host vs conspecific-parasitized host, P = 0.006; healthy host vs self-parasitized hosts, P = 0.008. parasitization rate: healthy host vs conspecific-parasitized host, P < 0.01; healthy host vs self-parasitized host, P < 0.001). It was indicated that parasitoid prefer parasitizing healthy host and avoiding superparasitism.
When A. prolixus facing both conspecific-parasitized and self-parasitized host, the behavioral parameters of A. prolixus on the two hosts have no significant differences (the number of hosts firstly contacted, P > 0.05; time for finding each host, P = 0.499; searching time, P = 0.612; probing time, P = 0.310; parasitization rate, P > 0.05). It was showed that A. prolixus couldn't discriminate between consecific-parasitized and self-parasitized host.
In non-choice tests, A. prolixus pefered parasitizing the healthy host (healthy host vs conspecific-parasitized host, P = 0.024; healthy host vs self-parasitized host, P = 0.010). It was also proved that the parasitoid marked the host in the process of prasitization. When there was only parasized host in the patch, the superparasitization rate of the previously parasitized host is 56%, but it is 14.3% when both healthy host and parasitized host were simultaneously provided to A. prolixus. It was indicated that A. prolixus could use parasitized hosts for parasitization when there is no healthy host available in the patch.
In choice tests, there were no significant differences in the behavioral parameters of A. prolixus between on the healthy host and on host with self-footprints or conspecific-footprints. (healthy host vs host with conspecific-footpints: the number of host firstly contacted, P > 0.05; time for finding each host, P = 0.476; searching time, P = 0.931; probing time, P = 0.420; parasitization rate, P > 0.05; healthy host vs host with self-footprints: the number of host firstly contacted, P > 0.05; time for finding each host, P = 0.931; searching time, P = 0.678; probing time, P = 0.859; parasitization rate, P > 0.05). It was indicated that A. prolixus couldn't discriminate between healthy host and host searched by conspecifc or itself and the parasitoid didn't marke the host when searching on the host (searching with antenna and probing with ovipositor).
When A. prolixus facing both healthy host and host previously parasitized but not smeared with ovipositor of the parsitoid , the behavioral parameters of A. prolixus on two kinds of hosts were not signicantly different(the number of each host firstly contacted, P > 0.05; time for contacting each host,P = 0.638; searching time,P = 0.538; probing time, P = 0.433; parasitization rate, P > 0.05). It was demonstrated that A. prolixus couldn't discriminate between healthy host and host parasized but not smeared with ovipositor of the parasitoid, and the parasioid didn't mark the host when searching, probing, detecting with ovipositor and ovipositing.
From the results above, It can be easily found that only the hosts smeared with ovipositor of A. prolixus have ovipositing marker, which is not physicalA mark but chemical mark, namely marking pheromones.
In the non-choice test, A. prolixus the parasitization rate on the healthy hosts are higher than hosts conspecific-parasitezed once or twice (healthy host vs host parasitezed once: P = 0.028; healthy host vs host parasitezed twice: P = 0.000). The parasitization rate on the conspecific parasitized once hosts is higher than hosts conspecific-parasitized twice (P = 0.013). It was indicated that more marking pheromones were accumulated on the host with times of parasitoid parasitizing the host increasing.
In the choice tests, the numbers of firstly contacted hosts applied dichloromethane extracts of the abdomen are significantly less than the controls (host applied dichloromethane) (P < 0.05). The searching time on the hosts applied dichloromethane extracts of the abdomen is significant less than the controls (P < 0.05). However, there were no significant differences between hosts applied other solvent extracts and the controls, which indicates that the marking pheromone is from the abdomen of the parasitoid and dichloromethane is the optimal solvent.
The results from GC-MS analysis showed that five groups of chemicals, including hydrocarbons, aldehydes, fatty acids, esters and terpenes, were found in the dichloromethane extracts of abdomen. The contents of hydrocarbons compounds consisting of 20 Akinds of chemicals is 40.55%, and aldehydes 3 kinds 0.32%, fatty acids 7 kinds 54.96%, esters 2 kinds 3.7% and terpenes 2 kinds 0.18%.
The bioassays were conducted to measure the effects of dichloromethane of extrats of the Dufour's gland, posion sac (gland) and ovaries of A. prolixus on the behavior of the parasitoid using choice tests The time for the parasitoid firstly contacting the hosts applied Dufour's glands was significantly more than control hosts (applied only dichloromethane) (P < 0.048). The searching time of the parasitoid on the host treated with the extracts of Dufour's gland was significantly less than control host(P = 0.039). The parasitization rate of host applied extracts of Dufour's gland was also lower than control host(P < 0.001). However, there were no significant differences between the controls and hosts applied posion sac (gland) or ovaries in behavioral parameters. It shows that the extracts of Dufour's gland have repellent and ovipostion-deterrent effects to the A. prolixus. The behavioral evidence suggests that Dufour's gland is the host marking pheromone source.
In the choice tests, it was found that the parasitization rate on the controls (host applied dichloromethane) was significantly higher than the hosts applied 10μg tetracosane (P < 0.05), and the numbers of the controls firstly contacted are higher than the hosts treated with 10μg palmitic acid (P < 0.05). However, 1μg palmitic acid, 1μg tetracosane, hexadecane (1μg and 10μg) and heptacosane (1μg and 10μg) have no effects on the host discrimination, which indicates palmitic acid and tetracosane are important components of marking pheromones.
在正常刻槽与某种已寄生刻槽(它蜂寄生或自己寄生的刻槽)同时存在的条件下,雌蜂首先接触到正常刻槽的次数明显高于已寄生刻槽(正常-它蜂寄生:P < 0.01,正常-自己寄生:P < 0.001),找到正常刻槽的时间明显少于已寄生刻槽(正常-它蜂寄生:P < 0.001,正常-自己寄生:P = 0.008),这表明桑天牛卵啮小蜂在寄生过程中的某个(或某些)环节对刻槽进行了标记,而这种标记物在近距离内被桑天牛卵啮小蜂感知,并对该寄生蜂产生趋避作用,使其优先选择正常刻槽;寄生蜂在正常刻槽上的搜索时间、刺探时间和寄生率也都明显高于已寄生刻槽(搜索时间:正常-它蜂寄生P = 0.002,正常-自己寄生P = 0.006;刺探时间:正常-它蜂寄生P = 0.006,正常-自己寄生P = 0.008;寄生率:正常-它蜂寄生P < 0.01,正常-自己寄生P < 0.001)。说明在正常刻槽和某种已寄生刻槽同时存在时,桑天牛卵啮小蜂优先寄生正常刻槽,避免过寄生。
当它蜂寄生和自己寄生刻槽都存在时,桑天牛卵啮小蜂对这两种已寄生刻槽的行为参数间没有显著性差异(接触到两种刻槽的次数:P > 0.05;找到刻槽所需时间:P = 0.499;搜索时间:P = 0.612;刺探时间:P = 0.310;寄生率:P > 0.05),这表明桑天牛卵啮小蜂不具有区分它蜂寄生刻槽和自己寄生刻槽的能力。
在非选择实验中,与已寄生刻槽(它蜂或自己寄生刻槽)相比,卵啮小蜂更易于在正常刻槽上产卵寄生(正常-它蜂:P = 0.024;正常-自己:P = 0.010),这再次证明了桑天牛卵啮小蜂在寄生过程中对刻槽进行了标记。当雌蜂只能面对某种已寄生刻槽时,其过寄生率为56%;而在有正常刻槽可供选择的情况下,已被寄生刻槽的寄生率为14.3%,这表明在没有正常刻槽存在时,卵啮小蜂也会利用已被寄生的刻槽。
通过选择实验发现,卵啮小蜂对正常刻槽和有爬行痕迹刻槽的行为参数间无显著差异(正常刻槽-有它蜂爬行痕迹刻槽:刻槽首先被接触到的次数,P > 0.05;找到每种刻槽所需时间,P = 0.476;搜索时间,P = 0.931;刺探时间,P = 0.420;寄生率,P > 0.05;正常刻槽-有自己爬行痕迹刻槽:刻槽首先被接触到的次数,P > 0.05;找到每种刻槽所需时间,P = 0.931;搜索时间,P = 0.678;刺探时间,P = 0.859;寄生率,P > 0.05)。这表明卵啮小蜂不能区分正常刻槽和被自己或其他个体搜索过的刻槽,说明卵啮小蜂在搜索过程中(包括触角搜索和产卵器刺探行为)没有标记刻槽。
当桑天牛卵啮小蜂同时面对正常刻槽和已被寄生但未被寄生蜂产卵器涂抹的刻槽时,每种刻槽首先被寄生蜂接触到的次数没有明显差别(P > 0.05),寄生蜂接触到每种刻槽所需要的时间也无显著差异(P = 0.638),在两种刻槽上的搜索时间、刺探时间以及寄生率等方面均无明显差异(搜索时间,P = 0.538;刺探时间,P = 0.433;寄生率,P > 0.05),说明卵啮小蜂不能识别正常刻槽和已被寄生但未被寄生蜂产卵器涂抹的刻槽。同时也表明,在寄生过程中,寄生蜂在刻槽表面搜索、刺探、产卵器对桑天牛卵检测、产卵均未对刻槽表面及刻槽内的桑天牛卵进行标记。
综合以上实验结果不难发现,只有被桑天牛卵啮小蜂产卵器涂抹后的刻槽上具有产卵标记,这种涂抹行为不会对刻槽表面产生物理标记,只能是化学标记,即标记信息素。
通过非选择实验发现,桑天牛卵啮小蜂在正常刻槽上的寄生率明显高于被寄生一次或寄生两次的刻槽(正常-它蜂寄生一次:P = 0.028;正常-它蜂寄生两次:P = 0.000),在被寄生一次刻槽上的寄生率明显高于寄生两次的刻槽(P = 0.013)。这表明随着刻槽被寄生次数的增多,在刻槽表面累积的标记信息素也增多。
对桑天牛卵啮小蜂雌蜂头、胸、腹部提取物的生测实验中,首次接触到滴加二氯甲烷的小蜂腹部提取物的刻槽的次数明显少于对照刻槽(只滴加二氯甲烷溶剂的正常刻槽)(P < 0.05),在滴加二氯甲烷的小蜂腹部提取物的刻槽上的搜索时间明显少于对照刻槽(P < 0.05) ,而滴加其他溶剂提取物的刻槽与对照相比则无显著差异,表明该寄生蜂标记信息素来源于寄生蜂腹部,且二氯甲烷为提取该寄生蜂标记素的最佳溶剂。
GC-MS(气相色谱-质谱联用仪)结果表明,桑天牛卵啮小蜂腹部的二氯甲烷提取物包括烃类、醛类、脂肪酸、酯类和萜类等5类化合物。烃类物质有20种,含量为40.55%,;醛类物质有3种,含量为0.32%;含有7种脂肪酸,含量为54.96%;酯类化合物为2种,含量为3.7%,萜类物质两种,含量为0.18%。
在对桑天牛卵啮小蜂杜氏腺、毒囊毒腺、卵巢的二氯甲烷提取物的生物测定实验中,寄生蜂找到对照刻槽的时间明显少于滴加杜氏腺提取液的刻槽(P = 0.048),在对照刻槽上的搜索时间明显多于滴加杜氏腺提取液的刻槽(P = 0.039),在对照刻槽上的寄生率也高于滴加杜氏腺提取液的刻槽(P < 0.001)。而寄生蜂在滴加毒囊毒腺或卵巢提取物刻槽上的行为参数与对照刻槽相比没有显著差异,这表明杜氏腺的提取物对卵啮小蜂有趋避和抑制产卵的作用,说明桑天牛卵啮小蜂的标记信息素来源于杜氏腺。
通过选择实验发现,桑天牛卵啮小蜂在对照刻槽(滴加二氯甲烷溶剂)上的寄生率明显高于滴加10μg二十四烷的刻槽(P < 0.05),首次接触到对照刻槽的次数明显多于滴加10μg棕榈酸的刻槽(P < 0.05),而1μg的棕榈酸和1μg二十四烷、十六烷(1μg和10μg)和二十七烷(1μg和10μg)对卵啮小蜂的寄主识别行为没有影响,说明棕榈酸和二十四烷为卵啮小蜂的标记信息素的重要组分。
Aprostocetus prolixus is an important egg parasitoid of A. germari, stem borer infesting many species of trees. This paper investigated the chemical mechanism in discrimination of previously prarasitized hosts by the parasitoid, which is very important to reveal the mechanism of parasitization by A. prolixus and use the parasitoid to control A. germari.
When the healthy host and the host previously parasitized (conspecific-parasitized or self-parasitized) in the same pacth, the number of healthy host firstly contacted is significantly higher than the previously parasitized host (healthy host vs conspecific-parasitized, P < 0.01; healthy hosts vs self-parasitized, P < 0.001). The time for A. prolixus finding healthy host was much less than that for searching previously prarsitized host (healthy host vs conspecific-parasitized host, P < 0.001; healthy host vs self-parasitized host, P < 0.008). It was demonstrated that A. prolixus had marked the host in some stage of the process of parasitization.The markers can be perceived by the parasitoid in short distance and have repellent effect to herself or other individuals, which make the parasitoid prefer choosing the healthy host. The searching time, probing time and parasitization rate were significantly higher than previously parasitized hosts (searching time: healthy host vs conspecific-parasitized host, P = 0.002; healthy hosts vs self-parasitized host: P = 0.006. probing time: healthy host vs conspecific-parasitized host, P = 0.006; healthy host vs self-parasitized hosts, P = 0.008. parasitization rate: healthy host vs conspecific-parasitized host, P < 0.01; healthy host vs self-parasitized host, P < 0.001). It was indicated that parasitoid prefer parasitizing healthy host and avoiding superparasitism.
When A. prolixus facing both conspecific-parasitized and self-parasitized host, the behavioral parameters of A. prolixus on the two hosts have no significant differences (the number of hosts firstly contacted, P > 0.05; time for finding each host, P = 0.499; searching time, P = 0.612; probing time, P = 0.310; parasitization rate, P > 0.05). It was showed that A. prolixus couldn't discriminate between consecific-parasitized and self-parasitized host.
In non-choice tests, A. prolixus pefered parasitizing the healthy host (healthy host vs conspecific-parasitized host, P = 0.024; healthy host vs self-parasitized host, P = 0.010). It was also proved that the parasitoid marked the host in the process of prasitization. When there was only parasized host in the patch, the superparasitization rate of the previously parasitized host is 56%, but it is 14.3% when both healthy host and parasitized host were simultaneously provided to A. prolixus. It was indicated that A. prolixus could use parasitized hosts for parasitization when there is no healthy host available in the patch.
In choice tests, there were no significant differences in the behavioral parameters of A. prolixus between on the healthy host and on host with self-footprints or conspecific-footprints. (healthy host vs host with conspecific-footpints: the number of host firstly contacted, P > 0.05; time for finding each host, P = 0.476; searching time, P = 0.931; probing time, P = 0.420; parasitization rate, P > 0.05; healthy host vs host with self-footprints: the number of host firstly contacted, P > 0.05; time for finding each host, P = 0.931; searching time, P = 0.678; probing time, P = 0.859; parasitization rate, P > 0.05). It was indicated that A. prolixus couldn't discriminate between healthy host and host searched by conspecifc or itself and the parasitoid didn't marke the host when searching on the host (searching with antenna and probing with ovipositor).
When A. prolixus facing both healthy host and host previously parasitized but not smeared with ovipositor of the parsitoid , the behavioral parameters of A. prolixus on two kinds of hosts were not signicantly different(the number of each host firstly contacted, P > 0.05; time for contacting each host,P = 0.638; searching time,P = 0.538; probing time, P = 0.433; parasitization rate, P > 0.05). It was demonstrated that A. prolixus couldn't discriminate between healthy host and host parasized but not smeared with ovipositor of the parasitoid, and the parasioid didn't mark the host when searching, probing, detecting with ovipositor and ovipositing.
From the results above, It can be easily found that only the hosts smeared with ovipositor of A. prolixus have ovipositing marker, which is not physicalA mark but chemical mark, namely marking pheromones.
In the non-choice test, A. prolixus the parasitization rate on the healthy hosts are higher than hosts conspecific-parasitezed once or twice (healthy host vs host parasitezed once: P = 0.028; healthy host vs host parasitezed twice: P = 0.000). The parasitization rate on the conspecific parasitized once hosts is higher than hosts conspecific-parasitized twice (P = 0.013). It was indicated that more marking pheromones were accumulated on the host with times of parasitoid parasitizing the host increasing.
In the choice tests, the numbers of firstly contacted hosts applied dichloromethane extracts of the abdomen are significantly less than the controls (host applied dichloromethane) (P < 0.05). The searching time on the hosts applied dichloromethane extracts of the abdomen is significant less than the controls (P < 0.05). However, there were no significant differences between hosts applied other solvent extracts and the controls, which indicates that the marking pheromone is from the abdomen of the parasitoid and dichloromethane is the optimal solvent.
The results from GC-MS analysis showed that five groups of chemicals, including hydrocarbons, aldehydes, fatty acids, esters and terpenes, were found in the dichloromethane extracts of abdomen. The contents of hydrocarbons compounds consisting of 20 Akinds of chemicals is 40.55%, and aldehydes 3 kinds 0.32%, fatty acids 7 kinds 54.96%, esters 2 kinds 3.7% and terpenes 2 kinds 0.18%.
The bioassays were conducted to measure the effects of dichloromethane of extrats of the Dufour's gland, posion sac (gland) and ovaries of A. prolixus on the behavior of the parasitoid using choice tests The time for the parasitoid firstly contacting the hosts applied Dufour's glands was significantly more than control hosts (applied only dichloromethane) (P < 0.048). The searching time of the parasitoid on the host treated with the extracts of Dufour's gland was significantly less than control host(P = 0.039). The parasitization rate of host applied extracts of Dufour's gland was also lower than control host(P < 0.001). However, there were no significant differences between the controls and hosts applied posion sac (gland) or ovaries in behavioral parameters. It shows that the extracts of Dufour's gland have repellent and ovipostion-deterrent effects to the A. prolixus. The behavioral evidence suggests that Dufour's gland is the host marking pheromone source.
In the choice tests, it was found that the parasitization rate on the controls (host applied dichloromethane) was significantly higher than the hosts applied 10μg tetracosane (P < 0.05), and the numbers of the controls firstly contacted are higher than the hosts treated with 10μg palmitic acid (P < 0.05). However, 1μg palmitic acid, 1μg tetracosane, hexadecane (1μg and 10μg) and heptacosane (1μg and 10μg) have no effects on the host discrimination, which indicates palmitic acid and tetracosane are important components of marking pheromones.
引文
[1] Harvey J A, Harvey I F, Thompson D J. The effect of superparasitism on development of the solitary parasitoid wasp, Venturia canescens [J]. Ecol. Entomol., 1993, 18: 203–208.
[2] Godfray H C J. Parasitoids: Behavioral and Evolutionary Ecology [M]. Princeton University Press, New Jersey. 1994.
[3] Ueno T. Effects of superparasitism, larval competition, and host–feeding in the pupal parasitoid Pimpla nipponica (Hymenoptera: Ichneumonidae) on offspring survival and fitness [J]. Ann. Entomol. Soc. Am., 1997, 90: 682–688.
[4] van Lenteren J C. Host discrimination by parasitoids. In: D.A. Nordlund, R. L. Jones & W. J. Lewis (eds), Semiochemicals.Their Role in Pest Control. Wiley, New York, pp.1981, 153–173.
[5] Hofsvang T. Discrimination between unparasitized and parasitized hosts in hymenopterous parasitoids [J]. Acta Entomologica Bohemoslovaca, 1990, 87: 161–175.
[6] C′esar R Nufio, Daniel R Papaj.Host marking behavior in phytophagous insects and parasitoids [J].Entomologia Experimentalis et Applicata, 2001, 99: 273–293.
[7] Corbet S A. Concentration effects and response of Nemeritis canescens to a secretion of its host [J]. Journal of Insect Physiology, 1973, 19: 2119–2128.
[8] Prokopy R J. Epideictic pheromones that influence spacing patterns of phytophagous insects. In: D.A. Nordlund, R.L. Jones, W. J. Lewis (eds), Semiochemicals: Their Role in Pest Control. Wiley Press, New York, pp. 1981,181–213.
[9] Rosi M C, Isidoro N, Colazza S,et al. Source of the host marking pheromone in the egg parasitoid Trissolcus basalis(Hymenoptera:Scelionidae) [J].Journal of Insect Physiology, 2001, 47: 989-995.
[10] Ikawa T, Okabe H. Regulation of egg number per host to maximize the reproductive success in the gregarious parasitoid, Apanteles glomeratus L (Hymenoptera: Braconidae) [J]. Applied Entomology and Zoology, 1985, 20: 331–339.
[11] Papaj D R , Roitberg B D, Opp S B, et al. Effect of marking pheromone on clutch size in the Mediterranean fruit fly [J]. Physiological Entomology, 1990, 15: 463–468.
[12] Bakker K , Eijsackers H J P, van Lenteren J C, et al. Some models describing distribution of eggs of parasite Pseudeucoila bochei (Hymenoptera: Cynipidae) over its hosts, larvae of Drosophila melanogaster [J]. Oecologia, 1972, 10: 29–57.
[13] Vinson S B. The behavior of parasitoids. In: Kerkut WJ, Gilbert LI, eds. Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon Press, NewYork. 1985.
[14] Roitberg B D, Cairl R S, Prokopy R J. Oviposition deterring pheromone influences dispersal distance in tephritid fruit flies[J]. Entomologia Experimentalis et Applicata, 1984, 35: 217–220.
[15] Roitberg B D, R J Prokopy. Insects that mark host plants [J]. Bioscience,1987, 37: 400–406.
[16] Roitberg B D, Mangel M. On the evolutionary ecology of marking pheromones [J]. Evolutionary Ecology, 1988, 2: 289–315.
[17] Price P W. Trail odors– recognition by insects parasitic on cocoons [J]. Science, 1970, 170: 546–547.
[18] Sugimoto T, Uenishi M, Machida F. Foraging for patchily distributed leaf-miners by the parasitoid, Dapsilarthra rufiventris (Hymenoptera: Braconidae). I. Discrimination of previously searched leaflets [J]. Applied Entomology and Zoology, 1986, 21: 500–508.
[19] Sheehan W, Wackers F L, Lewis W J. Discrimination of previously searched, host-free sites by Microplitis croceipes (Hymenoptera: Braconidae) [J]. Journal of Insect Behavior, 1993, 6: 323– 331.
[20] Holmes H B. Genetic evidence for fewer progeny and a higher percent males when Nasonia vitripennis oviposites in previously parasitized hosts [J]. Entomophaga, 1972, 17: 79–88.
[21] van Alphen J J M, Thunnissen I. Host selection and sex allocation by Pachycrepoideus vindemiae Rondani (Pteromalidae) as a facultative hyperparasitoid of Asobara tabida Nees (Braconidae; Alysiinae) and Leptopilina heterotoma (Cynipoidea; Eucoilidae) [J]. Netherlands Journal of Zoology, 1983, 33: 497–514.
[22] Waage J K , Lane J A. The reproductive strategy of a parasitic wasp. II. Sex allocation and local mate competition in Trichogramma evanescens [J]. Journal of Animal Ecology, 1984, 53: 417– 426.
[23] Field S A, Keller M A, G Calbert. The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defence [J]. Ecological Entomology, 1997, 22: 142–149.
[24] Salt G. Experimental studies in insect parasitism. V. The sense used by Trichogramma to distinguish between parasitized and unparasitized hosts. Proceedings of the Royal Society of London, Series B-Biological Sciences, 1937, 122: 57–75.
[25] van Lenteren J C. The development of host discrimination and the prevention of superparasitism in the parasite Pseudeucoila bochei Weld (Hymenoptera: Cynipidae) [J]. Netherlands Journal of Zoology, 1976, 26: 1–83.
[26] Chabi Olaye A,Schulthess G,Poehling H M, et al. Host location and host diacrimination behavior of Telenomus isis,an egg parasitoid of the African cereal stem borer Sesamis calamistis [J].Chem.Ecol., 2001, 27: 663–677.
[27]Rabinovich J E, Jorda M T, Bemstein C. Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera:Scelionidae), a parasitoid of triatomine eggs [J].Behav. Ecol. Sociobiol., 2000, 48:308–315.
[28] Okuda M S, Yeargan K V.Habitat partitioning by Telenomus podisi and Trissolcus euschisti (Hymenoptera:Scelionidae) between heraceous and woody host plants.Environ.Entomol., 1988, 17: 795–798.
[29] Wiedemann L M, Canto Silva C R,Romanowski H P, et al. Oviposition behaviour of Gryon gallardoi (Hym.:Scelionidae) on eggs of Spartocera dentiventris (Hem.:Coreidae) [J].Braz. J. Biol., 2003, 63: 133–139.
[30] Wu Z X,Nordlund D A.Superparasitism of Lygus hesperus Knight eggs by Anaphes iole Girault inthe laboratory [J].Biol.Control, 2002, 23: 121–126.
[31] van Baaren J,Boivin G,Nenon J P.Intra- and interspecific host discrimination in two closely related egg parasitoids [J].Oecologia, 1994, 100: 325–330.
[32] Guillot F S, Vinson S B. Sources of substances which elicit a behavioural response from insect parasitoid, Campoletis perdistinctus [J]. Nature, 1972, 235: 169–170.
[33] Guillot F S,Joiner R S,Vinson S B.Host discrimination of hydrocarbon from the Dufor’s gland of a braconid parasitoid [J]. Ann. Entomol. Soc. Amer., 1974, 67: 720–721.
[34] Hoffmeister T S,Gienapp P. Discrimination against previously searched, host-free patches by a parasitoid foraging for concealed hosts [J]. Ecological Entomology,2001,26, 487–494.
[35] Sugimoto T, Tsujimoto S. Stopping rule of host search by the parasitoid, Chrysocharis pentheus (Hymenoptera: Eulophidae), in host patches [J]. Res. Popul. Ecol. 1988,30, 123–133.
[36] Sugimoto T, Minkenberg O P J M , Takabayashi J.et al.1990 Foraging for patchily-distributed leaf miners by the parasitic wasp, Dacnusa sibirica [J]. Res. Popul. Ecol. 1990,32, 381–389.
[37] Greany P D, Oatman E R. Analysis of host discrimination in parasite Orgilus lepidus (Hymenoptera: Braconidae) [J]. Annals of the Entomological Society of America, 1972, 65: 377–383.
[38] Galis F, van Alphen J J M. Patch time allocation and search intensity of Asobara tabida Nees (Braconidae), a larval parasitoid of Drosophila [J]. Neth. J. Zool. 1981, 31, 596–611.
[39] van Dijken M J, van Stratum P, van Alphen J J M. Recognition of individual-specific marked parasitized hosts by the solitary parasitoid Epidinocarsis lopezi [J]. Behavioral Ecology and Sociobiology, 1992, 30: 77–82.
[40] van Baaren J, Nenon J P. Host location and discrimination mediated through olfactory stimuli in two species of Encyrtidae[J]. Entomologia Experimentalis et Applicata,1996, 81: 61–69.
[41] Kouloussis N A , B I Katsoyannos. Host discrimination and evidence for a host marking pheromone in the almond seed wasp, Eurytoma amygdali [J]. Entomologia Experimentalis et Applicata, 1991, 58: 165–174.
[42] van Lenteren J C. Contact-chemoreceptors on the ovipositor of Pseudeucoila bochei Weld (Cynipidae). Netherlands Journal of Zoology, 1972, 22: 347–350.
[43] Ganesalingam V K. Mechanism of discrimination between parasitized and unparasitized hosts by Venturia canescens (Hymenoptera: Ichneumonidae) [J]. Entomologia Experimentalis et Applicata, 1974, 17: 36–44.
[44] King P E, Rafai J. Host discrimination in a gregarious parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) [J]. Journal of Experimental Biology, 1970,53: 245–254.
[45] Hilker M, Klein B. Investigation of oviposition deterrent in larval frass of Spodoptera littoralis (Boisd) [J]. Journal of Chemical Ecology, 1989, 15: 929–938.
[46] Ferguson A W, Ziesmann J, Blight M M,et al. Perception of oviposition-deterring pheromone by cabbage seed weevil (Ceutorhynchus assimilis) [J]. Journal of Chemical Ecology,1999, 25: 1655–1670.
[47] Bosque C, Rabinovich J E. Population dynamics of Telenomus fariai (Hymenoptera, Scelionidae),a parasite of Chagas disease vectors. VII. oviposition behavior and host discrimination [J]. Canadian Entomologist , 1979,111: 171–180.
[49] Hoffmeister T S, Roitberg B D. To mark the host or the patch: Decisions of a parasitoid searching for concealed host larvae [J]. Evolutionary Ecology, 1997, 11: 145–168.
[48] Gross P. Insect behavioral and morphological defenses against parasitoids [J]. Annual Review of Entomology,1993, 38: 251–273.
[50] CHEN Hua Cai,CHENG Jia An.Insect host marking pheromones [J].Acta Ecologica Sinica, 2005, 25 (2): 346–35.
[51] Gauthier N, Monge J P. Could the egg itself be the source of the oviposition deterrent marker in the ectoparasitoid Dinarmus basalis [J]? Journal of Insect Physiology, 1999, 45: 393–400.
[52] Visser M. E, Luyckx B, Nell H W, et al. Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism [J]. Ecological Entomology, 1992, 17: 76–82.
[53] Nelson J M, Roitberg B D.Factors governing host discrimination by Opius dimidiatus (Ashmead) (Hymenoptera: Braconidae) [J]. Journal of Insect Behavior,1993, 6: 13–24.
[54] Strand M R. The physiological interactions of parasitoids with their hosts and the influence on reproductive strategies. In: J. K. Waage & D. Greathead (eds), Insect Parasitoids. Academic Press, London, pp., 1986, 97–136.
[55] H?ller C , Williams H J, Vinson S B. Evidence for a 2-component external marking pheromone system in an aphid hyperparasitoid [J]. Journal of Chemical Ecology, 1991, 17: 1021–1035.
[56] Chow F J, Mackauer M. Host discrimination and larval competition in the aphid parasite Ephedrus californicus [J]. Entomologia Experimentalis et Applicata, 1986, 41: 243–254.
[57] Cloutier C,Dohse L A,Bauduin F. Host discrimination in the aphid parasitoid Aphidius nigripes [J]. Canadian Journal of Zoology-Revue Canadienne de Zoologie, 1984, 62: 1367–1372.
[58] Gauthier N, Monge J P. Could the egg itself be the source of the oviposition deterrent marker in the ectoparasitoid Dinarmus basalis [J]? Journal of Insect Physiology, 1999, 45: 393–400.
[59] Alejandro Tena, Apostolos Kapranas, Ferran Garcia-Mari, et al. Host discrimination, superparasitism and infanticide by a gregarious endoparasitoid [J].Animal behaviour, 2008, 76, 789-799.
[60] Strand M R, Godfray H C J. Superparasitism and ovicide in parasitic Hymenoptera: A case study of the ectoparasitoid Bracon hebetor [J]. Behavioral Ecology and Sociobiology, 1989, 24: 421–432.
[61] Mayhew P J. Fitness consequences of ovicide in a parasitoid wasp [J]. Entomologia Experimentalis et Applicata, 1997, 84: 115–126.
[62] Mudd A, Fisher R C , Smith M C. Volatile hydrocarbons in the Dufour's gland of the parasite Nemeritis canescens (Grav.) (Hymenoptera: Ichneumonidae) [J]. Journal of Chemical Ecology, 1982, 8: 1035–1042.
[63] Bragg D E. Ecological and behavioral studies of Phaeogenes cynarae: ecology; host specificity; searching and oviposition; and avoidance of superparasitism [J] Annals of the EntomologicalSociety of America, 1974,67: 931–936.
[64] Yamaguchi H. The role of venom in host discrimination of Ascogaster reticulatus Watanabe [J]. Japanese Journal of Applied Entomology and Zoology, 1987, 31: 80–82.
[65] H?ller C, Bargen H, Vinson S B, et al. Sources of the marking pheromones used for host discrimination in the hyperparasitoid Dendrocerus carpenteri [J]. Journal of Insect Physiology, 1993, 39: 649–656.
[66] Ganesalingam V K. Mechanism of discrimination between parasitized and unparasitized hosts by Venturia canescens (Hymenoptera: Ichneumonidae) [J]. Entomologia Experimentalis et Applicata, 1974, 17: 36–44.
[67] Marris G C, Hubbard S F, Scrimgeour C. The perception of genetic similarity by the solitary parthenogenetic parasitoid Venturia canescens, and its effects on the occurrence of superparasitism [J]. Entomologia Experimentalis et Applicata , 1996, 78: 167–174.
[68] Syvertsen T C, Jacckson L L, Blomquist G J, et al. Alkadienes mediating courtship in the parasitoid Cardiochiles nigriceps(Hymenoptera:Braconidae) [J]. Chem. Ecol., 1995, 21: 1971–1989.
[69] Howard R W, Baker J E, Morgan E D. Novel diterpenoids and hydrocarbons in the Dufour's gland of the ectoparasitoid Habrobracon hebetor(Say)(Hymenoptera:Braconidae) [J]. Arch. Insect Biochem. Physiol., 2003, 54: 95–109.
[70] Baker J, Howard R, Morrill W, et al. Acetate esters of saturated and unsaturated alcohols(C12-C20) are major components in Dufour's glands of Bracon cephi and Bracon lissogaster (Hymenoptera: Braconidae), parasitoid of the wheat stem sawfly, Cephus cinctus(Hymenoptera:Cephidae) [J]. Biochem. Syst. Ecol., 2005, 33: 757–769.
[71] Howard R W, Baker J E. Morphology and chemistry of Dufour's glands in four Ectoparasitoids: Cephalonomia tarsalis, C. waterstoni(Hymenoptera: Bethylidae), Anisopteromalus calandrae, and Pteromalus cerealellae(Hymenoptera: Pteromalidae) [J]. Comp.Biochem.Physiol.B, 2003, 135:153–167.
[72] Bouskila A,Robertson I C , Robinson , et al . Submaximal oviposition rates in a mymarid parasitoid: choosiness should not be ignored [J] . Ecology, 1995, 76 , 1990–1993 .
[73] Strand M R, Obrycki J J. Host specifi city of insect parasitoids and predators [J] . Bioscience , 1996, 46, 422–429 .
[74] Clark C W, Mangel M . Dynamic State Variable Models in Ecology: Methods and Applications . Oxford University Press , New York . 2000.
[75] Fletcher J P , Hughes J P, Harvey I F. Life expectancy and egg load affect oviposition decisions of a solitary parasitoid [J]. Proceedings of the Royal Society of London Series B, 1994,258, 163–167 .
[76] Islam K S, Copland M J. Influence of egg load and oviposition time interval on the host discrimination and offspring survival of Anagyrus pseudococci(Hymenoptera:Encurtidae), a solitary endoparasitoid of citrus mealybug, Planococcus citri (Hemipera:Pseudococcidae) [J].Bull. Entomol. Res., 2000, 90: 6 9–75.
[77] Bai B. Conspecific super-parasitism in two parasitoid wasps, Aphidius ervi Haliday and Aphidius asychis Walker: reproductive strategies in Xuence host discrimination [J]. Can. Entomol., 1991, 123, 1229–1237.
[78] Babendreier D, Hoffmeister T S. Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate [J]. Entomol. Expt. Appl., 2002, 105: 63–69.
[79] V·lkl W, Mackauer M. Age-specific pattern of host discrimination by the aphid parasitoid Ephedrus californicus Baker (Hymenoptera: Aphidiidae) [J]. Canadian Entomologist, 1990, 122: 349–361.
[80] Visser M E. The influence of competition between foragers on clutch size decisions in an insect parasitoid with scramble larval competition [J]. Behavioral Ecology, 1996, 7: 109–114.
[81] Hubbard S F, Harvey I F, Fletcher J P. Avoidance of superparasitism: a matter of learning [J]? Animal Behaviour, 1999, 57: 1193–1197.
[82] Dukas R, Duan J J. Potential fitness consequences of associative learning in a parasitoid wasp. Behav. Ecol., 2000, 11: 536–543.
[83] Grasswitz T R. Effect of adult experience on the host-location behavior of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphi diidae) [J].Biol.Control, 1998,12: 177–181.
[84] Ardeh M J, de Jong P W, van Lenteren J C. Intra- and interspecific host discrimination in arrhenotokous and thelytokous Eretomocerus spp. Biol. Control, 2005, 33: 74–80.
[85] Papaj D R, Vet L E M. Odor learning and foraging success in the parasitoid, Leptopilina heterotoma [J]. Chem.Ecol.,1990,16: 3137–3150.
[86] Bakker K, van Alphen J J M, van Batenburg F H D, et al.The function of host discrimination and superparasitization in parasitoids [J]. Oecologia, 1985, 67: 572–576.
[87] Field S A, Keller M A, G Calbert. The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defence [J]. Ecological Entomology, 1997, 22: 142–149.
[88] Bartlett B R, Ball J C. The developmental biologies of two encyrtid parasites of Coccus hesperidum and their intrinsic competition [J]. Annals of the Entomological Society of America, 1964, 57, 496–503.
[89] Marlène Goubault, Manuel Plantegenest, Denis Poinsot, et al. Effect of expected offspring survival probability on host selection in a solitary parasitoid [J].The Netherlands Entomological Society Entomologia Experimentalis et Applicata, 2003, 109: 123–131.
[90] van Alphen J J M, Visser M E. Superparasitism as an adaptive strategy for insect parasitoids [J]. Annual Review of Entomology, 1990,35: 59–79.
[91]黄大庄.1999.桑天牛区域动态规律与综合治理[M].哈尔滨:东北林业大学出版社.
[92] Hoffmeister T S. Marking decisions and host discrimination in a parasitoid attacking concealed hosts [J]. Can. J. Zool., 2000, 78 (8): 1494–1499.
[93]李继泉,王树香,杨元,黄大庄,金幼菊,白颖.桑天牛长尾啮小蜂产卵及寄主识别行为的观察与研究[J].蚕业科学, 2006, 32 (4): 447–452.
[94] Segoli M, Keasar T, Bouskila A, Harari A. Host choice decisions in the polyembryonic waspCopidosoma koehleri (Hymenoptera: Encyrtidae) [J]. Physiol. Entomol., 2010, 35, 40–45.
[95] McKay T, Broce A B. Discrimination of Self-Parasitized Hosts by the Pupal Parasitoid Muscidifurax zaraptor (Hymenoptera: Pteromalidae) [J]. Ann. Entomol. Soc. Am., 2004, 97 (3): 592–599.
[96] Ueno T, Tanaka T. Self-host discrimination by a parasitic wasp: the role of short-term memory [J]. Anim. Behav., 1996, 52 (5): 875–883.
[97] Castillo A, Infante F, Vera-graziano J, Trujillo J. Host-discrimination by Phymastichus coffea, a parasitoid of the coffee berry borer [J]. Biocontrol, 2004, 49: 655–663.
[98] Bernstein C, Driessen G. Patch-marking and optimal search patterns in the parasitoid Venturia canescens [J]. Anim. Ecol., 1996, 65: 211–219.
[99] Fisher R C, Ganesalingam V K.Changes in the composition of host haemolymph after attack by an insect parasitoid [J]. Nature, 1970, 227: 190–192.
[100] Stelinski L L, Oakleaf R, Rodriguez-Saona C. Oviposition-deterring pheromone deposited on blueberry fruit by the parasitic wasp, Diachasma alloeum [J]. Behaviour, 2007, 144(4): 429–445.
[101] Field S A, Keller M A. Short-term host discrimination in the parasitoid wasp Trissolcus basalis Wollaston (Hymenoptera: Scelionidae) [J]. Aust. Zool., 1999, 47: 19–28.
[102] Agboka K, Schulthess F, Chabi-Olaye A, et al. Self-, intra-, and interspecific host discrimination in Telenomus busseolae Gahan and T. isis Polaszek (Hymenoptera: Scelionidae), sympatric egg parasitoids of the African cereal stem borer, Sesamia calamistis Hampson (Lepidoptera: Noctuidae) [J]. Insect Behav., 2002, 15: 1–12.
[103] Foltyn S, Gerling D. The parasitoids of the aleyrodid Bemisia tabaci in Israel: development, host preference and discrimination of the Aphelinid wasp Eretmocerus mundus [J]. Entomologia Experimentalis et Applicata, 1985, 38: 255–260.
[104] White R A., Agosin M, Franklin R T, et al. Bark beetle pheromones: evidence for physiological synthesis mechanisms and their ecological implications [J]. Zeitschrift für Angewandte Entomologie, 1980, 90: 255–274.
[105] Quiring D T, Sweeney J W, Bennett R G. Evidence for a host-marking pheromone in white spruce cone fly, Strobilomyia neanthracina [J]. Journal of Chemical Ecology, 1998, 24: 709–721.
[2] Godfray H C J. Parasitoids: Behavioral and Evolutionary Ecology [M]. Princeton University Press, New Jersey. 1994.
[3] Ueno T. Effects of superparasitism, larval competition, and host–feeding in the pupal parasitoid Pimpla nipponica (Hymenoptera: Ichneumonidae) on offspring survival and fitness [J]. Ann. Entomol. Soc. Am., 1997, 90: 682–688.
[4] van Lenteren J C. Host discrimination by parasitoids. In: D.A. Nordlund, R. L. Jones & W. J. Lewis (eds), Semiochemicals.Their Role in Pest Control. Wiley, New York, pp.1981, 153–173.
[5] Hofsvang T. Discrimination between unparasitized and parasitized hosts in hymenopterous parasitoids [J]. Acta Entomologica Bohemoslovaca, 1990, 87: 161–175.
[6] C′esar R Nufio, Daniel R Papaj.Host marking behavior in phytophagous insects and parasitoids [J].Entomologia Experimentalis et Applicata, 2001, 99: 273–293.
[7] Corbet S A. Concentration effects and response of Nemeritis canescens to a secretion of its host [J]. Journal of Insect Physiology, 1973, 19: 2119–2128.
[8] Prokopy R J. Epideictic pheromones that influence spacing patterns of phytophagous insects. In: D.A. Nordlund, R.L. Jones, W. J. Lewis (eds), Semiochemicals: Their Role in Pest Control. Wiley Press, New York, pp. 1981,181–213.
[9] Rosi M C, Isidoro N, Colazza S,et al. Source of the host marking pheromone in the egg parasitoid Trissolcus basalis(Hymenoptera:Scelionidae) [J].Journal of Insect Physiology, 2001, 47: 989-995.
[10] Ikawa T, Okabe H. Regulation of egg number per host to maximize the reproductive success in the gregarious parasitoid, Apanteles glomeratus L (Hymenoptera: Braconidae) [J]. Applied Entomology and Zoology, 1985, 20: 331–339.
[11] Papaj D R , Roitberg B D, Opp S B, et al. Effect of marking pheromone on clutch size in the Mediterranean fruit fly [J]. Physiological Entomology, 1990, 15: 463–468.
[12] Bakker K , Eijsackers H J P, van Lenteren J C, et al. Some models describing distribution of eggs of parasite Pseudeucoila bochei (Hymenoptera: Cynipidae) over its hosts, larvae of Drosophila melanogaster [J]. Oecologia, 1972, 10: 29–57.
[13] Vinson S B. The behavior of parasitoids. In: Kerkut WJ, Gilbert LI, eds. Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon Press, NewYork. 1985.
[14] Roitberg B D, Cairl R S, Prokopy R J. Oviposition deterring pheromone influences dispersal distance in tephritid fruit flies[J]. Entomologia Experimentalis et Applicata, 1984, 35: 217–220.
[15] Roitberg B D, R J Prokopy. Insects that mark host plants [J]. Bioscience,1987, 37: 400–406.
[16] Roitberg B D, Mangel M. On the evolutionary ecology of marking pheromones [J]. Evolutionary Ecology, 1988, 2: 289–315.
[17] Price P W. Trail odors– recognition by insects parasitic on cocoons [J]. Science, 1970, 170: 546–547.
[18] Sugimoto T, Uenishi M, Machida F. Foraging for patchily distributed leaf-miners by the parasitoid, Dapsilarthra rufiventris (Hymenoptera: Braconidae). I. Discrimination of previously searched leaflets [J]. Applied Entomology and Zoology, 1986, 21: 500–508.
[19] Sheehan W, Wackers F L, Lewis W J. Discrimination of previously searched, host-free sites by Microplitis croceipes (Hymenoptera: Braconidae) [J]. Journal of Insect Behavior, 1993, 6: 323– 331.
[20] Holmes H B. Genetic evidence for fewer progeny and a higher percent males when Nasonia vitripennis oviposites in previously parasitized hosts [J]. Entomophaga, 1972, 17: 79–88.
[21] van Alphen J J M, Thunnissen I. Host selection and sex allocation by Pachycrepoideus vindemiae Rondani (Pteromalidae) as a facultative hyperparasitoid of Asobara tabida Nees (Braconidae; Alysiinae) and Leptopilina heterotoma (Cynipoidea; Eucoilidae) [J]. Netherlands Journal of Zoology, 1983, 33: 497–514.
[22] Waage J K , Lane J A. The reproductive strategy of a parasitic wasp. II. Sex allocation and local mate competition in Trichogramma evanescens [J]. Journal of Animal Ecology, 1984, 53: 417– 426.
[23] Field S A, Keller M A, G Calbert. The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defence [J]. Ecological Entomology, 1997, 22: 142–149.
[24] Salt G. Experimental studies in insect parasitism. V. The sense used by Trichogramma to distinguish between parasitized and unparasitized hosts. Proceedings of the Royal Society of London, Series B-Biological Sciences, 1937, 122: 57–75.
[25] van Lenteren J C. The development of host discrimination and the prevention of superparasitism in the parasite Pseudeucoila bochei Weld (Hymenoptera: Cynipidae) [J]. Netherlands Journal of Zoology, 1976, 26: 1–83.
[26] Chabi Olaye A,Schulthess G,Poehling H M, et al. Host location and host diacrimination behavior of Telenomus isis,an egg parasitoid of the African cereal stem borer Sesamis calamistis [J].Chem.Ecol., 2001, 27: 663–677.
[27]Rabinovich J E, Jorda M T, Bemstein C. Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera:Scelionidae), a parasitoid of triatomine eggs [J].Behav. Ecol. Sociobiol., 2000, 48:308–315.
[28] Okuda M S, Yeargan K V.Habitat partitioning by Telenomus podisi and Trissolcus euschisti (Hymenoptera:Scelionidae) between heraceous and woody host plants.Environ.Entomol., 1988, 17: 795–798.
[29] Wiedemann L M, Canto Silva C R,Romanowski H P, et al. Oviposition behaviour of Gryon gallardoi (Hym.:Scelionidae) on eggs of Spartocera dentiventris (Hem.:Coreidae) [J].Braz. J. Biol., 2003, 63: 133–139.
[30] Wu Z X,Nordlund D A.Superparasitism of Lygus hesperus Knight eggs by Anaphes iole Girault inthe laboratory [J].Biol.Control, 2002, 23: 121–126.
[31] van Baaren J,Boivin G,Nenon J P.Intra- and interspecific host discrimination in two closely related egg parasitoids [J].Oecologia, 1994, 100: 325–330.
[32] Guillot F S, Vinson S B. Sources of substances which elicit a behavioural response from insect parasitoid, Campoletis perdistinctus [J]. Nature, 1972, 235: 169–170.
[33] Guillot F S,Joiner R S,Vinson S B.Host discrimination of hydrocarbon from the Dufor’s gland of a braconid parasitoid [J]. Ann. Entomol. Soc. Amer., 1974, 67: 720–721.
[34] Hoffmeister T S,Gienapp P. Discrimination against previously searched, host-free patches by a parasitoid foraging for concealed hosts [J]. Ecological Entomology,2001,26, 487–494.
[35] Sugimoto T, Tsujimoto S. Stopping rule of host search by the parasitoid, Chrysocharis pentheus (Hymenoptera: Eulophidae), in host patches [J]. Res. Popul. Ecol. 1988,30, 123–133.
[36] Sugimoto T, Minkenberg O P J M , Takabayashi J.et al.1990 Foraging for patchily-distributed leaf miners by the parasitic wasp, Dacnusa sibirica [J]. Res. Popul. Ecol. 1990,32, 381–389.
[37] Greany P D, Oatman E R. Analysis of host discrimination in parasite Orgilus lepidus (Hymenoptera: Braconidae) [J]. Annals of the Entomological Society of America, 1972, 65: 377–383.
[38] Galis F, van Alphen J J M. Patch time allocation and search intensity of Asobara tabida Nees (Braconidae), a larval parasitoid of Drosophila [J]. Neth. J. Zool. 1981, 31, 596–611.
[39] van Dijken M J, van Stratum P, van Alphen J J M. Recognition of individual-specific marked parasitized hosts by the solitary parasitoid Epidinocarsis lopezi [J]. Behavioral Ecology and Sociobiology, 1992, 30: 77–82.
[40] van Baaren J, Nenon J P. Host location and discrimination mediated through olfactory stimuli in two species of Encyrtidae[J]. Entomologia Experimentalis et Applicata,1996, 81: 61–69.
[41] Kouloussis N A , B I Katsoyannos. Host discrimination and evidence for a host marking pheromone in the almond seed wasp, Eurytoma amygdali [J]. Entomologia Experimentalis et Applicata, 1991, 58: 165–174.
[42] van Lenteren J C. Contact-chemoreceptors on the ovipositor of Pseudeucoila bochei Weld (Cynipidae). Netherlands Journal of Zoology, 1972, 22: 347–350.
[43] Ganesalingam V K. Mechanism of discrimination between parasitized and unparasitized hosts by Venturia canescens (Hymenoptera: Ichneumonidae) [J]. Entomologia Experimentalis et Applicata, 1974, 17: 36–44.
[44] King P E, Rafai J. Host discrimination in a gregarious parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) [J]. Journal of Experimental Biology, 1970,53: 245–254.
[45] Hilker M, Klein B. Investigation of oviposition deterrent in larval frass of Spodoptera littoralis (Boisd) [J]. Journal of Chemical Ecology, 1989, 15: 929–938.
[46] Ferguson A W, Ziesmann J, Blight M M,et al. Perception of oviposition-deterring pheromone by cabbage seed weevil (Ceutorhynchus assimilis) [J]. Journal of Chemical Ecology,1999, 25: 1655–1670.
[47] Bosque C, Rabinovich J E. Population dynamics of Telenomus fariai (Hymenoptera, Scelionidae),a parasite of Chagas disease vectors. VII. oviposition behavior and host discrimination [J]. Canadian Entomologist , 1979,111: 171–180.
[49] Hoffmeister T S, Roitberg B D. To mark the host or the patch: Decisions of a parasitoid searching for concealed host larvae [J]. Evolutionary Ecology, 1997, 11: 145–168.
[48] Gross P. Insect behavioral and morphological defenses against parasitoids [J]. Annual Review of Entomology,1993, 38: 251–273.
[50] CHEN Hua Cai,CHENG Jia An.Insect host marking pheromones [J].Acta Ecologica Sinica, 2005, 25 (2): 346–35.
[51] Gauthier N, Monge J P. Could the egg itself be the source of the oviposition deterrent marker in the ectoparasitoid Dinarmus basalis [J]? Journal of Insect Physiology, 1999, 45: 393–400.
[52] Visser M. E, Luyckx B, Nell H W, et al. Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism [J]. Ecological Entomology, 1992, 17: 76–82.
[53] Nelson J M, Roitberg B D.Factors governing host discrimination by Opius dimidiatus (Ashmead) (Hymenoptera: Braconidae) [J]. Journal of Insect Behavior,1993, 6: 13–24.
[54] Strand M R. The physiological interactions of parasitoids with their hosts and the influence on reproductive strategies. In: J. K. Waage & D. Greathead (eds), Insect Parasitoids. Academic Press, London, pp., 1986, 97–136.
[55] H?ller C , Williams H J, Vinson S B. Evidence for a 2-component external marking pheromone system in an aphid hyperparasitoid [J]. Journal of Chemical Ecology, 1991, 17: 1021–1035.
[56] Chow F J, Mackauer M. Host discrimination and larval competition in the aphid parasite Ephedrus californicus [J]. Entomologia Experimentalis et Applicata, 1986, 41: 243–254.
[57] Cloutier C,Dohse L A,Bauduin F. Host discrimination in the aphid parasitoid Aphidius nigripes [J]. Canadian Journal of Zoology-Revue Canadienne de Zoologie, 1984, 62: 1367–1372.
[58] Gauthier N, Monge J P. Could the egg itself be the source of the oviposition deterrent marker in the ectoparasitoid Dinarmus basalis [J]? Journal of Insect Physiology, 1999, 45: 393–400.
[59] Alejandro Tena, Apostolos Kapranas, Ferran Garcia-Mari, et al. Host discrimination, superparasitism and infanticide by a gregarious endoparasitoid [J].Animal behaviour, 2008, 76, 789-799.
[60] Strand M R, Godfray H C J. Superparasitism and ovicide in parasitic Hymenoptera: A case study of the ectoparasitoid Bracon hebetor [J]. Behavioral Ecology and Sociobiology, 1989, 24: 421–432.
[61] Mayhew P J. Fitness consequences of ovicide in a parasitoid wasp [J]. Entomologia Experimentalis et Applicata, 1997, 84: 115–126.
[62] Mudd A, Fisher R C , Smith M C. Volatile hydrocarbons in the Dufour's gland of the parasite Nemeritis canescens (Grav.) (Hymenoptera: Ichneumonidae) [J]. Journal of Chemical Ecology, 1982, 8: 1035–1042.
[63] Bragg D E. Ecological and behavioral studies of Phaeogenes cynarae: ecology; host specificity; searching and oviposition; and avoidance of superparasitism [J] Annals of the EntomologicalSociety of America, 1974,67: 931–936.
[64] Yamaguchi H. The role of venom in host discrimination of Ascogaster reticulatus Watanabe [J]. Japanese Journal of Applied Entomology and Zoology, 1987, 31: 80–82.
[65] H?ller C, Bargen H, Vinson S B, et al. Sources of the marking pheromones used for host discrimination in the hyperparasitoid Dendrocerus carpenteri [J]. Journal of Insect Physiology, 1993, 39: 649–656.
[66] Ganesalingam V K. Mechanism of discrimination between parasitized and unparasitized hosts by Venturia canescens (Hymenoptera: Ichneumonidae) [J]. Entomologia Experimentalis et Applicata, 1974, 17: 36–44.
[67] Marris G C, Hubbard S F, Scrimgeour C. The perception of genetic similarity by the solitary parthenogenetic parasitoid Venturia canescens, and its effects on the occurrence of superparasitism [J]. Entomologia Experimentalis et Applicata , 1996, 78: 167–174.
[68] Syvertsen T C, Jacckson L L, Blomquist G J, et al. Alkadienes mediating courtship in the parasitoid Cardiochiles nigriceps(Hymenoptera:Braconidae) [J]. Chem. Ecol., 1995, 21: 1971–1989.
[69] Howard R W, Baker J E, Morgan E D. Novel diterpenoids and hydrocarbons in the Dufour's gland of the ectoparasitoid Habrobracon hebetor(Say)(Hymenoptera:Braconidae) [J]. Arch. Insect Biochem. Physiol., 2003, 54: 95–109.
[70] Baker J, Howard R, Morrill W, et al. Acetate esters of saturated and unsaturated alcohols(C12-C20) are major components in Dufour's glands of Bracon cephi and Bracon lissogaster (Hymenoptera: Braconidae), parasitoid of the wheat stem sawfly, Cephus cinctus(Hymenoptera:Cephidae) [J]. Biochem. Syst. Ecol., 2005, 33: 757–769.
[71] Howard R W, Baker J E. Morphology and chemistry of Dufour's glands in four Ectoparasitoids: Cephalonomia tarsalis, C. waterstoni(Hymenoptera: Bethylidae), Anisopteromalus calandrae, and Pteromalus cerealellae(Hymenoptera: Pteromalidae) [J]. Comp.Biochem.Physiol.B, 2003, 135:153–167.
[72] Bouskila A,Robertson I C , Robinson , et al . Submaximal oviposition rates in a mymarid parasitoid: choosiness should not be ignored [J] . Ecology, 1995, 76 , 1990–1993 .
[73] Strand M R, Obrycki J J. Host specifi city of insect parasitoids and predators [J] . Bioscience , 1996, 46, 422–429 .
[74] Clark C W, Mangel M . Dynamic State Variable Models in Ecology: Methods and Applications . Oxford University Press , New York . 2000.
[75] Fletcher J P , Hughes J P, Harvey I F. Life expectancy and egg load affect oviposition decisions of a solitary parasitoid [J]. Proceedings of the Royal Society of London Series B, 1994,258, 163–167 .
[76] Islam K S, Copland M J. Influence of egg load and oviposition time interval on the host discrimination and offspring survival of Anagyrus pseudococci(Hymenoptera:Encurtidae), a solitary endoparasitoid of citrus mealybug, Planococcus citri (Hemipera:Pseudococcidae) [J].Bull. Entomol. Res., 2000, 90: 6 9–75.
[77] Bai B. Conspecific super-parasitism in two parasitoid wasps, Aphidius ervi Haliday and Aphidius asychis Walker: reproductive strategies in Xuence host discrimination [J]. Can. Entomol., 1991, 123, 1229–1237.
[78] Babendreier D, Hoffmeister T S. Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate [J]. Entomol. Expt. Appl., 2002, 105: 63–69.
[79] V·lkl W, Mackauer M. Age-specific pattern of host discrimination by the aphid parasitoid Ephedrus californicus Baker (Hymenoptera: Aphidiidae) [J]. Canadian Entomologist, 1990, 122: 349–361.
[80] Visser M E. The influence of competition between foragers on clutch size decisions in an insect parasitoid with scramble larval competition [J]. Behavioral Ecology, 1996, 7: 109–114.
[81] Hubbard S F, Harvey I F, Fletcher J P. Avoidance of superparasitism: a matter of learning [J]? Animal Behaviour, 1999, 57: 1193–1197.
[82] Dukas R, Duan J J. Potential fitness consequences of associative learning in a parasitoid wasp. Behav. Ecol., 2000, 11: 536–543.
[83] Grasswitz T R. Effect of adult experience on the host-location behavior of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphi diidae) [J].Biol.Control, 1998,12: 177–181.
[84] Ardeh M J, de Jong P W, van Lenteren J C. Intra- and interspecific host discrimination in arrhenotokous and thelytokous Eretomocerus spp. Biol. Control, 2005, 33: 74–80.
[85] Papaj D R, Vet L E M. Odor learning and foraging success in the parasitoid, Leptopilina heterotoma [J]. Chem.Ecol.,1990,16: 3137–3150.
[86] Bakker K, van Alphen J J M, van Batenburg F H D, et al.The function of host discrimination and superparasitization in parasitoids [J]. Oecologia, 1985, 67: 572–576.
[87] Field S A, Keller M A, G Calbert. The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defence [J]. Ecological Entomology, 1997, 22: 142–149.
[88] Bartlett B R, Ball J C. The developmental biologies of two encyrtid parasites of Coccus hesperidum and their intrinsic competition [J]. Annals of the Entomological Society of America, 1964, 57, 496–503.
[89] Marlène Goubault, Manuel Plantegenest, Denis Poinsot, et al. Effect of expected offspring survival probability on host selection in a solitary parasitoid [J].The Netherlands Entomological Society Entomologia Experimentalis et Applicata, 2003, 109: 123–131.
[90] van Alphen J J M, Visser M E. Superparasitism as an adaptive strategy for insect parasitoids [J]. Annual Review of Entomology, 1990,35: 59–79.
[91]黄大庄.1999.桑天牛区域动态规律与综合治理[M].哈尔滨:东北林业大学出版社.
[92] Hoffmeister T S. Marking decisions and host discrimination in a parasitoid attacking concealed hosts [J]. Can. J. Zool., 2000, 78 (8): 1494–1499.
[93]李继泉,王树香,杨元,黄大庄,金幼菊,白颖.桑天牛长尾啮小蜂产卵及寄主识别行为的观察与研究[J].蚕业科学, 2006, 32 (4): 447–452.
[94] Segoli M, Keasar T, Bouskila A, Harari A. Host choice decisions in the polyembryonic waspCopidosoma koehleri (Hymenoptera: Encyrtidae) [J]. Physiol. Entomol., 2010, 35, 40–45.
[95] McKay T, Broce A B. Discrimination of Self-Parasitized Hosts by the Pupal Parasitoid Muscidifurax zaraptor (Hymenoptera: Pteromalidae) [J]. Ann. Entomol. Soc. Am., 2004, 97 (3): 592–599.
[96] Ueno T, Tanaka T. Self-host discrimination by a parasitic wasp: the role of short-term memory [J]. Anim. Behav., 1996, 52 (5): 875–883.
[97] Castillo A, Infante F, Vera-graziano J, Trujillo J. Host-discrimination by Phymastichus coffea, a parasitoid of the coffee berry borer [J]. Biocontrol, 2004, 49: 655–663.
[98] Bernstein C, Driessen G. Patch-marking and optimal search patterns in the parasitoid Venturia canescens [J]. Anim. Ecol., 1996, 65: 211–219.
[99] Fisher R C, Ganesalingam V K.Changes in the composition of host haemolymph after attack by an insect parasitoid [J]. Nature, 1970, 227: 190–192.
[100] Stelinski L L, Oakleaf R, Rodriguez-Saona C. Oviposition-deterring pheromone deposited on blueberry fruit by the parasitic wasp, Diachasma alloeum [J]. Behaviour, 2007, 144(4): 429–445.
[101] Field S A, Keller M A. Short-term host discrimination in the parasitoid wasp Trissolcus basalis Wollaston (Hymenoptera: Scelionidae) [J]. Aust. Zool., 1999, 47: 19–28.
[102] Agboka K, Schulthess F, Chabi-Olaye A, et al. Self-, intra-, and interspecific host discrimination in Telenomus busseolae Gahan and T. isis Polaszek (Hymenoptera: Scelionidae), sympatric egg parasitoids of the African cereal stem borer, Sesamia calamistis Hampson (Lepidoptera: Noctuidae) [J]. Insect Behav., 2002, 15: 1–12.
[103] Foltyn S, Gerling D. The parasitoids of the aleyrodid Bemisia tabaci in Israel: development, host preference and discrimination of the Aphelinid wasp Eretmocerus mundus [J]. Entomologia Experimentalis et Applicata, 1985, 38: 255–260.
[104] White R A., Agosin M, Franklin R T, et al. Bark beetle pheromones: evidence for physiological synthesis mechanisms and their ecological implications [J]. Zeitschrift für Angewandte Entomologie, 1980, 90: 255–274.
[105] Quiring D T, Sweeney J W, Bennett R G. Evidence for a host-marking pheromone in white spruce cone fly, Strobilomyia neanthracina [J]. Journal of Chemical Ecology, 1998, 24: 709–721.