AbstractGreenhouse whitefly (Trialeurodes vaporariorum) is a major global pest, causing direct damage to plants and transmitting viral plant diseases. Management of T. vaporariorum is problematic because of widespread pesticide resistance, and many greenhouse growers rely on biological control agents to regulate T.

温室粉虱（Trialeurodes vaporariorum）是一种主要的全球害虫，对植物造成直接危害并传播病毒性植物疾病。T的管理。由于广泛的抗药性，vaporariorum存在问题，许多温室种植者依靠生物防治剂来调节T。

vaporariorum populations. However, these are often slow and vary in efficacy, leading to subsequent application of chemical insecticides when pest populations exceed threshold levels. Combining chemical and biological pesticides has great potential but can result in different outcomes, from positive to negative interactions.

vaporariorum种群。然而，这些通常缓慢且功效不同，导致当害虫种群超过阈值水平时，随后使用化学杀虫剂。化学和生物农药的结合具有很大的潜力，但可能会产生不同的结果，从正面到负面的相互作用。

In this study, we evaluated co-applications of the entomopathogenic fungi (EPF) Beauveria bassiana and Cordyceps farinosa and the chemical insecticide spiromesifen in laboratory bioassays. Complex interactions between the EPFs and insecticide were described using an ecotoxicological mixtures model, the MixTox analysis.

在这项研究中，我们评估了昆虫病原真菌（EPF）白僵菌（Beauveria bassiana）和冬虫夏草（Cordyceps farinosa）以及化学杀虫剂螺旋霉素（spiromesifen）在实验室生物测定中的共同应用。使用生态毒理学混合物模型MixTox分析描述了EPF和杀虫剂之间的复杂相互作用。

Depending on the EPF and chemical concentrations applied, mixtures resulted in additivity, synergism, or antagonism in terms of total whitefly mortality. Combinations of B. bassiana and spiromesifen, compared to single treatments, increased the rate of kill by 5 days. Results indicate the potential for combined applications of EPF and spiromesifen as an effective integrated pest management strategy and demonstrate the applicability of the MixTox model to describe complex mixture interactions..

。与单一处理相比，球孢白僵菌和螺旋霉烯的组合使杀灭率提高了5天。结果表明，EPF和螺霉烯作为一种有效的综合害虫管理策略的联合应用潜力，并证明了MixTox模型在描述复杂混合物相互作用方面的适用性。。

IntroductionThe greenhouse whitefly (Trialeurodes vaporariorum) is a major insect pest causing substantial damage to > 850 plant species, including high-value greenhouse, ornamental and agricultural crops1. Damage by T. vaporariorum is caused directly by feeding and through the transmission of plant viruses, resulting in crop losses in excess of $1 billion a year2,3,4.

引言温室粉虱（Trialeurodes vaporariorum）是一种主要的害虫，对850多种植物物种造成重大损害，包括高价值的温室，观赏和农业作物1。T.vaporariorum的损害是由植物病毒的饲养和传播直接引起的，每年导致作物损失超过10亿美元2,3,4。

The most effective greenhouse insect integrated pest management (IPM) systems are based on preventative applications of arthropod predators and parasitoids5 as components of an integrated pest management (IPM) ‘pyramid’ approach6. Under this system, IPM-compatible chemical plant protection products (PPPs) are still applied but are used as supplementary treatments to biological control, acting as a second line of defence should pest numbers increase to levels where natural enemies are unable to control them7.Increasingly, IPM practitioners in greenhouse crops are incorporating low-risk plant protection products such as microbial PPPs into their programmes.

最有效的温室昆虫综合害虫管理（IPM）系统是基于节肢动物捕食者和寄生虫的预防应用5，作为综合害虫管理（IPM）“金字塔”方法的组成部分6。。

These biopesticides are typically based on microorganisms such as entomopathogenic bacteria (predominantly Bacillus thuringiensis), viruses, fungi, and protozoa8. Microbial PPPs for control of T. vaporariorum and other species of whiteflies are based primarily on entomopathogenic fungi (EPF). Entomopathogenic fungi infect their host via direct penetration by conidia through the host cuticle and then via proliferation in the host, ultimately killing the insect in a few days.Microbial PPPs are selected to have high specificity to the insect pest but also have a number of advantages, including lack of toxic residues, shorter pre-harvest and re-entry intervals for workers, and the potential for a certain amount of self-sustaining secondary control through re.

这些生物杀虫剂通常基于微生物，如昆虫病原菌（主要是苏云金芽孢杆菌），病毒，真菌和原生动物8。用于控制T.vaporariorum和其他种类粉虱的微生物PPP主要基于昆虫病原真菌（EPF）。昆虫病原真菌通过分生孢子直接穿透宿主角质层，然后通过宿主增殖感染宿主，最终在几天内杀死昆虫。选择微生物PPP对害虫具有高度特异性，但也具有许多优点，包括缺乏有毒残留物，工人的收获前和重返间隔较短，以及通过重新进行一定程度的自我维持二级控制的潜力。

There were significant differences between the total mortality observed at the end of the 12d bioassay for each treatment in the mixture bioassays involving B. bassiana and spiromesifen (F = 16.36, df = 12, p =  < 0.001). In single-application treatments, mortality ranged from 2 to 90% depending on the concentration of EPF or spiromesifen applied, with increasing application concentration resulting in increasing mortality.

在涉及球孢双歧杆菌和螺霉烯的混合物生物测定中，每种处理在12d生物测定结束时观察到的总死亡率之间存在显着差异（F=16.36，df=12，p=0.001）。在单次施用治疗中，死亡率范围为2%至90%，具体取决于施用的EPF或螺霉烯的浓度，随着施用浓度的增加，死亡率增加。

There were no significant differences between mortality for each treatment across bioassays (F = 2.35, df = 2, p = 0.10) or conidia deposition for the application of the same EPF concentration (Table 3). Therefore, further analysis was conducted with data compiled as one dataset across all bioassays.

生物测定中每种处理的死亡率（F=2.35，df=2，p=0.10）或应用相同EPF浓度的分生孢子沉积之间没有显着差异（表3）。因此，对所有生物测定中汇编为一个数据集的数据进行了进一步分析。

Control mortality was 3.5%, 3.2%, and 10.6% in each bioassay respectively. Total corrected mortality ranged from 0.2 to 88%, depending on the treatment applied. For combined applications, mortality data were successfully described by the Independent action (IA) model (R2 = 0.63, p < 0.001), and the addition of parameters to allow for antagonism or synergism did not improve the fit (p = 0.73).

在每次生物测定中，对照死亡率分别为3.5%，3.2%和10.6%。根据所采用的治疗方法，总校正死亡率范围为0.2%至88%。对于组合应用，死亡率数据通过独立作用（IA）模型成功描述（R2=0.63，p<0.001），并且添加参数以允许拮抗或协同作用并没有改善拟合（p=0.73）。

Therefore, all mixture outcomes for concentrations applied of B. bassiana and spiromesifen resulted in additivity, whereby the observed mortality was not significantly different from the expected mortality based on the single dose response of each component, assuming they follow independent action, as shown in Fig. 2.Table 3 Average dose received by 22 × 22 mm coverslips during spray applications of lethal concentrations (LC) of Beauveria bassiana, spiromesifen or simultaneous applications of both control agents in three replicate mixture bioassays.Full size tableFigure 2Mixture interactions 14 days after the simultaneous application of Beauveria bassiana and spirome.

因此，球孢白僵菌和螺旋体霉素浓度的所有混合物结果都产生了加和性，因此观察到的死亡率与基于每种成分的单剂量反应的预期死亡率没有显着差异，假设它们遵循独立作用，如图2所示。表3在喷雾应用致命浓度（LC）的球孢白僵菌，螺旋体霉素或在三次重复混合物生物测定中同时应用两种对照剂期间，22×22 mm盖玻片接受的平均剂量。全尺寸表图2同时应用白僵菌和螺旋体后14天的混合物相互作用。

(1)

(1)

where a is the percentage mortality data from the treated group and b is the percentage mortality from the control group.Differences in total mortality at the end of the bioassay between treatments and between bioassays were determined by ANOVA in R studio (version 4.0.0 2020/04/24).The predicted combined effect of the two control agents was calculated from the single treatment applications assuming Bliss independence24.

其中a是治疗组的死亡率百分比数据，b是对照组的死亡率百分比。通过R studio（版本4.0.0 2020/04/24）中的ANOVA确定治疗之间和生物测定之间生物测定结束时总死亡率的差异。假设Bliss独立，从单一治疗应用计算两种对照剂的预测组合效应24。

Under this assumption, each control agent interacting in the mixture kills the target pest by a dissimilar mechanism. This method uses the combination of unaffected fractions to calculate the expected outcome of a mixture.$$Pm=\left(pA\right)(pB)$$.

在此假设下，混合物中相互作用的每种控制剂都通过不同的机制杀死目标害虫。该方法使用未受影响分数的组合来计算混合物的预期结果$$Pm=\左（pA \右）（pB）$$。

(2)

(2)

where the probability of an organism surviving the combined treatment of agent A and agent B (\(Pm\)) would be the probability of an organism surviving agent A (\(pA\)) multiplied by the probability of an organism surviving agent B (\(pB\)). Therefore, a mixture consisting of two agents which independently each cause 25% mortality when applied alone will result in 56% mortality as a mixture assuming no interaction between the agents (also known as additivity), by the calculation of (1 − 0.25) * (1 − 0.25) = 1 − survivorship.

其中，生物体存活的概率（药剂A和药剂B的联合处理）（\（Pm）\）将是生物体存活的概率（药剂A）（\（pA）\）乘以生物体存活的概率（药剂B）（\（pB）））。因此，通过计算（1-0.25）*（1-0.25）=1-survivorship，假设两种药物之间没有相互作用（也称为加和性），由两种药物组成的混合物单独使用时各自独立导致25%的死亡率将导致56%的死亡率。

If the observed mortality is greater than the expected mortality, a synergistic interaction has occurred. Alternatively, antagonism results in lower mortality than expected.The effect of pathogen—spiromesifen mixtures were determined using the MixTox analysis23. Mortality was modeled against dose received for EPF applications in order to account for variation in suspensions applied between replicates and bioassays.

如果观察到的死亡率大于预期死亡率，则发生了协同相互作用。另外，拮抗作用导致死亡率低于预期。使用MixTox分析确定病原体螺旋体混合物的作用23。根据EPF应用所接受的剂量对死亡率进行建模，以解释重复和生物测定之间应用的悬浮液的变化。

The MixTox analysis takes into account the control mortality, so uncorrected data was used for this analysis. In this analysis, a reference model is produced based on mortality observed following experiments to determine the mortality achieved with the single application of each mixture component. The reference model describes the expected outcome of applications of the mixture across a range of concentrations assuming independent action of components based on the single outcomes of the single applications.

。在此分析中，根据实验后观察到的死亡率产生参考模型，以确定每种混合物组分单次应用所达到的死亡率。参考模型描述了在一系列浓度范围内应用混合物的预期结果，假设基于单一应用的单一结果的组分的独立作用。

Mixture effects are characterised based on the deviation of observed mixture data compared to the independent action reference model (i.e., the expected outcomes). Deviations from the independent action model can differ across the model axes. Patterns in the deviation from the reference model can be categorised as absol.

。与独立动作模型的偏差可能在模型轴上有所不同。偏离参考模型的模式可以归类为绝对模式。

Data availability

数据可用性

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

在当前研究期间生成和/或分析的数据集可根据合理要求从通讯作者处获得。

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Download referencesAcknowledgementsThis study was funded by the Natural Environment Research Council (NERC) Industrial CASE (Collaborative Awards in Science and Engineering) studentship award granted to the Centre for Ecology and Hydrology (NERC grant reference: NE/P010490/1).The University of Warwick co-supervised the PhD and were the awarding University partner.

下载参考文献致谢本研究由自然环境研究委员会（NERC）工业案例（科学与工程合作奖）授予生态与水文中心的学生奖资助（NERC资助参考文献：NE/P010490/1）。华威大学共同监督博士学位，并成为授予博士学位的大学合作伙伴。

Additional funding and support as part of the award is provided by BASF (Industrial CASE Partner) and CAB International (Partner).Author informationAuthors and AffiliationsUK Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire, OX10 8BB, UKEleanor L.

作为该奖项的一部分，巴斯夫（工业案例合作伙伴）和CAB国际（合作伙伴）提供了额外的资金和支持。作者信息作者和附属机构生态与水文中心，麦克莱恩大厦，本森巷，克罗马什-吉福德，沃林福德，牛津郡，OX10 8BB，UKEleanor L。

Dearlove, Claus Svendsen & Helen HeskethRSK ADAS Ltd. ADAS Gleadthorpe, Meden Vale, Mansfield, NG20 9PD, UKEleanor L. DearloveWarwick Crop Centre, School of Life Sciences, Wellesbourne Campus, The University of Warwick, Warwick, UKDavid ChandlerCABI, Bakeham Lane, Egham, TW20 9TY, UKSteve EdgingtonCertis Biologicals, Columbia, MD, USAShaun D.

Dearlove，Claus Svendsen&Helen HeskethRSK ADAS Ltd.ADAS Gleadthorpe，Meden Vale，Mansfield，NG20 9PD，Ukelenor L.DearloveWarwick作物中心，生命科学学院，Wellesbourne校区，沃里克大学，沃里克，UKDavid ChandlerCABI，Bakeham Lane，Egham，TW20 9TY，UKSteve EdgingtonCertis Biologicals，Columbia，MD，USAShaun D。

BerryBASF Plc, Woolpit, UKGareth MartinAuthorsEleanor L. DearloveView author publicationsYou can also search for this author in.

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PubMed Google ScholarContributionsELD conducted experiments within the manuscript, gathered data, conducted statistical and wrote the manuscript, with additional review from HH. All authors provided guidance on experimental design and context for impact of results. All authors reviewed the final manuscript and provided input to iterative review, prior to submission.Corresponding authorsCorrespondence to.

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Reprints and permissionsAbout this articleCite this articleDearlove, E.L., Chandler, D., Edgington, S. et al. Improved control of Trialeurodes vaporariorum using mixture combinations of entomopathogenic fungi and the chemical insecticide spiromesifen.

转载和许可本文引用本文Dearlove，E.L.，Chandler，D.，Edgington，S。等人使用昆虫病原真菌和化学杀虫剂spiromesifen的混合物改进了对Trialeurodes vaporariorum的控制。

Sci Rep 14, 15259 (2024). https://doi.org/10.1038/s41598-024-66051-8Download citationReceived: 16 November 2023Accepted: 26 June 2024Published: 03 July 2024DOI: https://doi.org/10.1038/s41598-024-66051-8Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

Sci Rep 1415259（2024）。https://doi.org/10.1038/s41598-024-66051-8Download引文接收日期：2023年11月16日接收日期：2024年6月26日发布日期：2024年7月3日OI：https://doi.org/10.1038/s41598-024-66051-8Share本文与您共享以下链接的任何人都可以阅读此内容：获取可共享链接对不起，本文目前没有可共享的链接。复制到剪贴板。

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KeywordsMixTox model

关键词Mixtox模型

Trialeurodes vaporariorum

蒸汽三列菌

Microbial controlBiopesticideEntomopathogenic fungiInteractionsSynergyAntagonismAdditivityIPM

微生物控制生物农药致病菌相互作用synergyantagonismadditivityipm

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