黑豆蚜内共生菌与可疑柄瘤蚜茧蜂寄主选择和后代发育表现的相关性研究
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摘要
业已明确,蚜虫专性内共生细菌布赫纳什菌Buchnera对于宿主蚜虫的营养代谢具有重要的作用,两者已建立了长期的协同演化关系；而蚜茧蜂是一类专门寄生蚜虫的内寄生蜂,蚜虫与蚜茧蜂亦有着长期的协同演化历史,因此,推测蚜虫共生菌必然与蚜茧蜂存在着某种关系。前期研究已发现,蚜虫次生共生细菌与蚜虫抵抗蚜茧蜂存在着直接关系。而且有研究推测,蚜茧蜂的寄主选择可能与蚜虫专性共生菌动态有关。但迄今尚未见研究报道,直接验证蚜虫初生共生菌—布赫纳什细菌Buchnera aphidicola与蚜茧蜂生活史策略之间的联系。为了探究这一问题,本论文研究比较了可疑柄瘤蚜茧蜂Lysiphlebus ambiguus对有菌和无菌黑豆蚜Aphis fabae各个历期的寄生选择及其子代蜂发育的相关适合度特征。此外,大气变化(如CO2浓度升高)对寄生蜂与寄主的互作生态学研究刚刚开始,急需增加新的研究案例。对此研究了高C02浓度下可疑柄瘤蚜茧蜂对不同历期黑豆蚜的寄生选择及其后代发育表现。获得以下主要研究结果和结论。
1、进行预备试验,旨在检测供试蚜虫内共生细菌状态以及获得代表蚜茧蜂选择性的产卵器有效针刺数。利用已知的初生共生细菌蚜布赫纳什细菌dnaK基因序列AB159734.1,设计引物进行特异性PCR扩增,检测结果表明,用抗生素处理后的黑豆蚜体内的初生共生菌迅速凋亡。用次生共生细菌Hamiltonella defensa dnaK基因序列AB159735.1设计引物进行特异性PCR扩增,未发现黑豆蚜体内存在抵御蚜茧蜂寄生的次生共生细菌HHamiltonella defensa。所以,在供试蚜虫种群中排除了次生共生细菌对寄生蜂的可能作用。子代蜂在无菌蚜虫体内的存活率低于有菌蚜虫,不同历期蚜虫之间也存在差异,所得到的差异值为后续试验数据分析中计算有效针刺提供了依据。
2、进行非选择性试验,旨在观察可疑柄瘤蚜茧蜂对不同含菌状态、不同历期寄主蚜虫的寄生选择及其子代蜂表现。采用常用的抗生素利福平处理寄主蚜虫,使蚜虫初生共生菌迅速凋亡,称这些蚜虫为无菌蚜虫,未进行抗生素处理的蚜虫称为有菌蚜虫。在非选择条件下,分别将不同处理的各历期蚜虫暴露给可疑柄瘤蚜茧蜂寄生。结果表明,除1龄蚜虫外,各历期无菌蚜虫的体型显著小于有菌蚜虫。可疑柄瘤蚜茧蜂对2-4龄无菌和有菌寄主黑豆蚜的寄生率(用有效针刺率表示)存在显著差异,显著偏好2龄有菌寄主以及3龄和4龄无菌蚜虫；但在1龄和成蚜中未表现出显著差异。除4龄寄主外,寄生无菌蚜虫的子代蜂羽化率显著低于寄生有菌蚜虫。
与寄生有菌蚜虫相比,寄生无菌蚜虫的子代蜂发育时间(产卵至成虫羽化)显著延长；在有菌蚜虫中,寄生幼龄和成蚜的子代蜂发育时间短于寄生中间历期蚜虫；但在无菌蚜虫中,子代寄生蜂的发育时间随着寄主历期的增加而缩短。据此推测,蚜茧蜂在去除共生菌的寄主蚜虫中,发育所需营养受到一定限制,导致其表现出较低的适合度。从无菌和有菌寄主黑豆蚜中羽化的子代可疑柄瘤蚜茧蜂,在生殖力上无显著差异,均随寄主蚜虫历期的增长而增大。
3、进行选择性试验,旨在观察可疑柄瘤蚜茧蜂对有菌和无菌寄主黑豆蚜的选择偏好,并观察其子代蜂发育适合度表现。研究结果表明,在历期相同的无菌和有菌寄主黑豆蚜之间,可疑柄瘤蚜茧蜂对较高历期(4龄和成蚜)的有菌寄主表现出显著偏好,但从子代蜂幼虫存活率和性比看,无菌蚜虫与有菌蚜虫无显著差异；在体型大小相同、但历期和含菌状态不同(2龄有菌和4龄无菌)的寄主黑豆蚜之间,可疑柄瘤蚜茧蜂偏好2龄有菌蚜虫。然而在不同历期的无菌蚜虫之间,可疑柄瘤蚜茧蜂未表现显著偏好。据测推测,可疑柄瘤蚜茧蜂能鉴别出老龄的有菌和无菌黑豆蚜,但是当所提供的蚜虫体型大小相近时,初生共生菌似乎又不是可疑柄瘤蚜茧蜂完成发育的一个必要条件,共生菌缺失仅影响到蚜茧蜂在老龄无菌寄主黑豆蚜中的发育。
4、进行室内搜寻行为观察试验,旨在比较可疑柄瘤蚜茧蜂对无菌和有菌黑豆蚜斑块的寄主搜寻行为。可疑柄瘤蚜茧蜂对有菌寄主和无菌寄主斑块的选择比例无显著差异,在有菌寄主斑块和无菌寄主斑块上的搜寻时间和滞留时间没有显著差异。这些结果都说明,在室内罩笼的环境下,可疑柄瘤蚜茧蜂不能区分有菌和无菌寄主的斑块。
5、进行室内试验研究,旨在观察高浓度CO2(750μl/L)对可疑柄瘤蚜茧蜂的寄生选择及其子代蜂发育表现的影响。与在正常浓度CO2环境下相比,在高浓度CO2环境下黑豆蚜体型显著变小。结果表明,可疑柄瘤蚜茧蜂对高浓度CO2环境中的黑豆蚜的寄生率(用僵蚜率表示)随寄主历期增长呈现下降趋势,而羽化率和性比不受寄主历期影响。与正常CO2浓度相比,寄生高CO2浓度蚜虫的子代蜂发育表现为：(ⅰ)4龄和成蚜的寄生率显著降低；(ⅱ)3龄寄主的羽化率显著下降；(ⅲ)1龄寄主的雌性比显著降低；(ⅳ)体型显著增大；(ⅴ)在2龄-4龄寄主中的发育时间显著缩短。这些结果都表明,高浓度CO2对可疑柄瘤蚜茧蜂的僵蚜率、羽化率、性比、子代体型大小和发育时间均有显著的影响。
6、本论文研究获得以下创新性结论：(ⅰ)首次初步探明了蚜茧蜂生活史特性与蚜虫初生共生菌的关系,发现可疑柄瘤蚜茧蜂在产卵时能够识别出有、无共生菌的高龄黑豆蚜,而且这种选择与后代发育表现存在一定的一致性；(ⅱ)研究表明,高浓度CO2对可疑柄瘤蚜茧蜂的寄生及其后代发育均有显著的影响。丰富了有关大气变化对寄生蜂与寄主互作生态学影响的知识。
Numerous studies indicate that endosymbiontic bacteria Bushnera perform a pivotal function in nutritional physiology of host aphids. While close co-evolution between aphids and their endosymbionts, and between aphids and aphidiine parasitoids have been established, it is assumed that some association between endosymbionts of aphids and higher trophic aphid parasitoids should be susceptible to natural selection. This assumption has been supported by empirical studies that facultative endosymbiotic bacteria of aphids are linked to resistance of host aphids to their parasitoids. Though it was suggested that host-stage selection of parasitoids might be associated with state of endosymbiotic Bushnera of aphids, there has been no empirical studies to address the association between life history of parasitoids and primary endosymbiotic Buchnera aphidicola of host aphids. Accordingly this study was designed to compare parasitism of an aphid parasitoid Lysiphlebus ambiguus in relation to aposymbiotic and symbiotic host Aphis fabae, and developmental performances of progeny parasitoids from attacking the aphid cohorts. In addition, we studied effects of carbon dioxide enrichment on interactions between host A. fabae and its parasitoid L. ambiguus, which would provide us with insights into co-evolution between aphids and their parasitoids as affected by climate changes. The main results and conclusions are summarized as follows.
1. Exploratory experiments were carried out to diagnose endosymbiotic bacteria of host aphids and to obtain the correction coefficient between mummies and effective stings exercised by mother parasitoids. The experimental stock aphids were screened for the presence of primary endosymbiotic Buchr.era aphidicola and of facultative bacterium Hamiltonella defensa with diagnostic polymerase chain reaction (PCR). The primary endosymbiotic B. aphidicola was detected, but the facultative endosymbiotic H. defense was not found in the A.fabae stock used in our experiments. Therefore, H. defense was excluded in the effects of endosymbions in our experiments. Survival of progeny parasitoids differed between symbiotic and aposymbiotc aphids and between stages, which was used to deduce effective stings made by mother parasitoids.
2. Non-choice experiments were conducted to observe parasitism of host aphids, and performances of progeny parasitoids, as affected by host stages and endosymbiosis. The aphids were treated using antibiotic rifampicin to obtain aposymbiotic aphids.Aposymbiotic aphids were significantly smaller in body size than corresponding symbiotic aphids at all stages except the first in unparasitized aphids. However, the differences in body size between symbiotic and aposymbiotic aphids did not produce significant variation in parasitism as measured by number of mummies. Eclosion rates of parasitoid progeny from aposymbiotic hosts were significantly lower than from corresponding symbiotic aphids in the1st stage to adult except for the3rd stage. Though female progeny increased with host size of consecutive stages in symbiotic aphids, no significant variation in sex ratio was exhibited across host stages of aposymbiotic aphids. Development time from egg-to-adult of progeny was distinctly prolonged in aposymbiotic aphids, compared to that in the symbiotic. Parasitism of young nymphs and adults of symbiotic aphids produced a shorter development time than intermediate host stages, but development time of progeny decreased in a linear relationship with life stages of aposymbiotic aphids. Our study suggests that differences in mortality rates of male and female wasps during development is likely to have influenced secondary sex ratio in relation to aphid stage for aphid cohorts deprived of symbiotic bacteria, and that bacteria disruption in aposymbiotic aphids can produce deleterious effects on growth and development of progeny parasitoids.
3. A series of paired-choice experiments was conducted to explore the preference of the parasitoid L. ambiguus for symbiotic and aposymbiotic A. fabae, and the suitability of these hosts for progeny parasitoid development. When given a choice between symbiotic and aposymbiotic aphids of the same stage, the parasitoid significantly preferred the symbiotic over aposymbiotic aphids only for the later stages (L4and adult). The suitability of aposymbiotic aphids for parasitoid development was only significantly lower than that of symbiotic aphids in L1and L4stages. When given a choice between similar-sized symbiotic L2and aposymbiotic L4aphids, the parasitoid preferred the former. No significant differences in preference were demonstrated when the parasitoid was given a choice between different stages of aposymbiotic aphids. For the latter two paired-choice experiments, there was no evidence of differential host suitability as exhibit by adult emergence rate and progeny sex ratio, although sample sizes were small. While lifetime fecundity increased with aphid stage at the time of oviposition, there was no significant influence of previous development from symbiotic versus aposymbiotic aphids. These results suggest that while L. ambiguus can discriminate between symbiotic and aposymbiotic A. fabae during later stages and when the aphids are of a similar size, there is little evidence that the primary symbiont is needed for successful parasitoid development.
4. Foraging behaviors of L. ambiguus were studied in symbiotic and aposymbiotic black bean aphid patches on plant in a transparent cage. The results showed that symbiotic and aposymbiotic aphid patches were not significantly different in parasitism, number of visits, time of residence, and time of foraging. It suggests that L. ambiguus may not be able to discriminate between patches of symbiotic and aposymbiotic aphids.
5. Effects of elevated CO2(750μl l-1) on the development of the black bean aphid A. fabae, and on performances of parasitoids L. ambiguus, were studied in incubators. Aphids under elevated CO2were significantly smaller in body size as measured by hind tibia length than corresponding aphids under nomal conditions at all stages.Non-choice experiments showed that L. ambiguus parasitized all stages of A. fabae cohort from the elevated CO2, and mummy production rates decreased with host aphid stages. In comparison with progeny parasitoids attacking aphids from normal CO2, progeny parasitoids in aphids from the elevated CO2performed as that:(i) parasitization rate for the4th stage and adult aphids was significantly low;(ii) wasp emergence rate in the third stage host was low;(iii) female proportion was low in the first stage host;(iv) body size was large;(v) development time in the second to forth stage hosts was reduced. The results suggest that elevated CO2should influence L. ambiguus in parasitism with Aphis fabae and development of progeny parasittoids.
6. This study has produced innovative findings in following aspects,(i) Association between primary endosymbitoic bacteria of host aphids and parasitoids has being revealed for the first time, which is that Lysiphlebus ambiguus is able to discriminate against aposymbiotic hosts Aphis fabae at higher stages and such preference is inagreement with offspring performances,(ii) Elevated CO2can influence L. ambiguus in parasitism with Aphis fabae and development of progeny parasitoids, which contributes to our understanding of ecological interactions between parasitoids and their hosts, as affected by CO2enrichment with the climate change.
1、进行预备试验,旨在检测供试蚜虫内共生细菌状态以及获得代表蚜茧蜂选择性的产卵器有效针刺数。利用已知的初生共生细菌蚜布赫纳什细菌dnaK基因序列AB159734.1,设计引物进行特异性PCR扩增,检测结果表明,用抗生素处理后的黑豆蚜体内的初生共生菌迅速凋亡。用次生共生细菌Hamiltonella defensa dnaK基因序列AB159735.1设计引物进行特异性PCR扩增,未发现黑豆蚜体内存在抵御蚜茧蜂寄生的次生共生细菌HHamiltonella defensa。所以,在供试蚜虫种群中排除了次生共生细菌对寄生蜂的可能作用。子代蜂在无菌蚜虫体内的存活率低于有菌蚜虫,不同历期蚜虫之间也存在差异,所得到的差异值为后续试验数据分析中计算有效针刺提供了依据。
2、进行非选择性试验,旨在观察可疑柄瘤蚜茧蜂对不同含菌状态、不同历期寄主蚜虫的寄生选择及其子代蜂表现。采用常用的抗生素利福平处理寄主蚜虫,使蚜虫初生共生菌迅速凋亡,称这些蚜虫为无菌蚜虫,未进行抗生素处理的蚜虫称为有菌蚜虫。在非选择条件下,分别将不同处理的各历期蚜虫暴露给可疑柄瘤蚜茧蜂寄生。结果表明,除1龄蚜虫外,各历期无菌蚜虫的体型显著小于有菌蚜虫。可疑柄瘤蚜茧蜂对2-4龄无菌和有菌寄主黑豆蚜的寄生率(用有效针刺率表示)存在显著差异,显著偏好2龄有菌寄主以及3龄和4龄无菌蚜虫；但在1龄和成蚜中未表现出显著差异。除4龄寄主外,寄生无菌蚜虫的子代蜂羽化率显著低于寄生有菌蚜虫。
与寄生有菌蚜虫相比,寄生无菌蚜虫的子代蜂发育时间(产卵至成虫羽化)显著延长；在有菌蚜虫中,寄生幼龄和成蚜的子代蜂发育时间短于寄生中间历期蚜虫；但在无菌蚜虫中,子代寄生蜂的发育时间随着寄主历期的增加而缩短。据此推测,蚜茧蜂在去除共生菌的寄主蚜虫中,发育所需营养受到一定限制,导致其表现出较低的适合度。从无菌和有菌寄主黑豆蚜中羽化的子代可疑柄瘤蚜茧蜂,在生殖力上无显著差异,均随寄主蚜虫历期的增长而增大。
3、进行选择性试验,旨在观察可疑柄瘤蚜茧蜂对有菌和无菌寄主黑豆蚜的选择偏好,并观察其子代蜂发育适合度表现。研究结果表明,在历期相同的无菌和有菌寄主黑豆蚜之间,可疑柄瘤蚜茧蜂对较高历期(4龄和成蚜)的有菌寄主表现出显著偏好,但从子代蜂幼虫存活率和性比看,无菌蚜虫与有菌蚜虫无显著差异；在体型大小相同、但历期和含菌状态不同(2龄有菌和4龄无菌)的寄主黑豆蚜之间,可疑柄瘤蚜茧蜂偏好2龄有菌蚜虫。然而在不同历期的无菌蚜虫之间,可疑柄瘤蚜茧蜂未表现显著偏好。据测推测,可疑柄瘤蚜茧蜂能鉴别出老龄的有菌和无菌黑豆蚜,但是当所提供的蚜虫体型大小相近时,初生共生菌似乎又不是可疑柄瘤蚜茧蜂完成发育的一个必要条件,共生菌缺失仅影响到蚜茧蜂在老龄无菌寄主黑豆蚜中的发育。
4、进行室内搜寻行为观察试验,旨在比较可疑柄瘤蚜茧蜂对无菌和有菌黑豆蚜斑块的寄主搜寻行为。可疑柄瘤蚜茧蜂对有菌寄主和无菌寄主斑块的选择比例无显著差异,在有菌寄主斑块和无菌寄主斑块上的搜寻时间和滞留时间没有显著差异。这些结果都说明,在室内罩笼的环境下,可疑柄瘤蚜茧蜂不能区分有菌和无菌寄主的斑块。
5、进行室内试验研究,旨在观察高浓度CO2(750μl/L)对可疑柄瘤蚜茧蜂的寄生选择及其子代蜂发育表现的影响。与在正常浓度CO2环境下相比,在高浓度CO2环境下黑豆蚜体型显著变小。结果表明,可疑柄瘤蚜茧蜂对高浓度CO2环境中的黑豆蚜的寄生率(用僵蚜率表示)随寄主历期增长呈现下降趋势,而羽化率和性比不受寄主历期影响。与正常CO2浓度相比,寄生高CO2浓度蚜虫的子代蜂发育表现为：(ⅰ)4龄和成蚜的寄生率显著降低；(ⅱ)3龄寄主的羽化率显著下降；(ⅲ)1龄寄主的雌性比显著降低；(ⅳ)体型显著增大；(ⅴ)在2龄-4龄寄主中的发育时间显著缩短。这些结果都表明,高浓度CO2对可疑柄瘤蚜茧蜂的僵蚜率、羽化率、性比、子代体型大小和发育时间均有显著的影响。
6、本论文研究获得以下创新性结论：(ⅰ)首次初步探明了蚜茧蜂生活史特性与蚜虫初生共生菌的关系,发现可疑柄瘤蚜茧蜂在产卵时能够识别出有、无共生菌的高龄黑豆蚜,而且这种选择与后代发育表现存在一定的一致性；(ⅱ)研究表明,高浓度CO2对可疑柄瘤蚜茧蜂的寄生及其后代发育均有显著的影响。丰富了有关大气变化对寄生蜂与寄主互作生态学影响的知识。
Numerous studies indicate that endosymbiontic bacteria Bushnera perform a pivotal function in nutritional physiology of host aphids. While close co-evolution between aphids and their endosymbionts, and between aphids and aphidiine parasitoids have been established, it is assumed that some association between endosymbionts of aphids and higher trophic aphid parasitoids should be susceptible to natural selection. This assumption has been supported by empirical studies that facultative endosymbiotic bacteria of aphids are linked to resistance of host aphids to their parasitoids. Though it was suggested that host-stage selection of parasitoids might be associated with state of endosymbiotic Bushnera of aphids, there has been no empirical studies to address the association between life history of parasitoids and primary endosymbiotic Buchnera aphidicola of host aphids. Accordingly this study was designed to compare parasitism of an aphid parasitoid Lysiphlebus ambiguus in relation to aposymbiotic and symbiotic host Aphis fabae, and developmental performances of progeny parasitoids from attacking the aphid cohorts. In addition, we studied effects of carbon dioxide enrichment on interactions between host A. fabae and its parasitoid L. ambiguus, which would provide us with insights into co-evolution between aphids and their parasitoids as affected by climate changes. The main results and conclusions are summarized as follows.
1. Exploratory experiments were carried out to diagnose endosymbiotic bacteria of host aphids and to obtain the correction coefficient between mummies and effective stings exercised by mother parasitoids. The experimental stock aphids were screened for the presence of primary endosymbiotic Buchr.era aphidicola and of facultative bacterium Hamiltonella defensa with diagnostic polymerase chain reaction (PCR). The primary endosymbiotic B. aphidicola was detected, but the facultative endosymbiotic H. defense was not found in the A.fabae stock used in our experiments. Therefore, H. defense was excluded in the effects of endosymbions in our experiments. Survival of progeny parasitoids differed between symbiotic and aposymbiotc aphids and between stages, which was used to deduce effective stings made by mother parasitoids.
2. Non-choice experiments were conducted to observe parasitism of host aphids, and performances of progeny parasitoids, as affected by host stages and endosymbiosis. The aphids were treated using antibiotic rifampicin to obtain aposymbiotic aphids.Aposymbiotic aphids were significantly smaller in body size than corresponding symbiotic aphids at all stages except the first in unparasitized aphids. However, the differences in body size between symbiotic and aposymbiotic aphids did not produce significant variation in parasitism as measured by number of mummies. Eclosion rates of parasitoid progeny from aposymbiotic hosts were significantly lower than from corresponding symbiotic aphids in the1st stage to adult except for the3rd stage. Though female progeny increased with host size of consecutive stages in symbiotic aphids, no significant variation in sex ratio was exhibited across host stages of aposymbiotic aphids. Development time from egg-to-adult of progeny was distinctly prolonged in aposymbiotic aphids, compared to that in the symbiotic. Parasitism of young nymphs and adults of symbiotic aphids produced a shorter development time than intermediate host stages, but development time of progeny decreased in a linear relationship with life stages of aposymbiotic aphids. Our study suggests that differences in mortality rates of male and female wasps during development is likely to have influenced secondary sex ratio in relation to aphid stage for aphid cohorts deprived of symbiotic bacteria, and that bacteria disruption in aposymbiotic aphids can produce deleterious effects on growth and development of progeny parasitoids.
3. A series of paired-choice experiments was conducted to explore the preference of the parasitoid L. ambiguus for symbiotic and aposymbiotic A. fabae, and the suitability of these hosts for progeny parasitoid development. When given a choice between symbiotic and aposymbiotic aphids of the same stage, the parasitoid significantly preferred the symbiotic over aposymbiotic aphids only for the later stages (L4and adult). The suitability of aposymbiotic aphids for parasitoid development was only significantly lower than that of symbiotic aphids in L1and L4stages. When given a choice between similar-sized symbiotic L2and aposymbiotic L4aphids, the parasitoid preferred the former. No significant differences in preference were demonstrated when the parasitoid was given a choice between different stages of aposymbiotic aphids. For the latter two paired-choice experiments, there was no evidence of differential host suitability as exhibit by adult emergence rate and progeny sex ratio, although sample sizes were small. While lifetime fecundity increased with aphid stage at the time of oviposition, there was no significant influence of previous development from symbiotic versus aposymbiotic aphids. These results suggest that while L. ambiguus can discriminate between symbiotic and aposymbiotic A. fabae during later stages and when the aphids are of a similar size, there is little evidence that the primary symbiont is needed for successful parasitoid development.
4. Foraging behaviors of L. ambiguus were studied in symbiotic and aposymbiotic black bean aphid patches on plant in a transparent cage. The results showed that symbiotic and aposymbiotic aphid patches were not significantly different in parasitism, number of visits, time of residence, and time of foraging. It suggests that L. ambiguus may not be able to discriminate between patches of symbiotic and aposymbiotic aphids.
5. Effects of elevated CO2(750μl l-1) on the development of the black bean aphid A. fabae, and on performances of parasitoids L. ambiguus, were studied in incubators. Aphids under elevated CO2were significantly smaller in body size as measured by hind tibia length than corresponding aphids under nomal conditions at all stages.Non-choice experiments showed that L. ambiguus parasitized all stages of A. fabae cohort from the elevated CO2, and mummy production rates decreased with host aphid stages. In comparison with progeny parasitoids attacking aphids from normal CO2, progeny parasitoids in aphids from the elevated CO2performed as that:(i) parasitization rate for the4th stage and adult aphids was significantly low;(ii) wasp emergence rate in the third stage host was low;(iii) female proportion was low in the first stage host;(iv) body size was large;(v) development time in the second to forth stage hosts was reduced. The results suggest that elevated CO2should influence L. ambiguus in parasitism with Aphis fabae and development of progeny parasittoids.
6. This study has produced innovative findings in following aspects,(i) Association between primary endosymbitoic bacteria of host aphids and parasitoids has being revealed for the first time, which is that Lysiphlebus ambiguus is able to discriminate against aposymbiotic hosts Aphis fabae at higher stages and such preference is inagreement with offspring performances,(ii) Elevated CO2can influence L. ambiguus in parasitism with Aphis fabae and development of progeny parasitoids, which contributes to our understanding of ecological interactions between parasitoids and their hosts, as affected by CO2enrichment with the climate change.
引文
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