{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T20:01:37Z","timestamp":1784577697224,"version":"3.55.0"},"reference-count":111,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2021,7,30]],"date-time":"2021-07-30T00:00:00Z","timestamp":1627603200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>\n                    The tomato leaf miner (TLM),\n                    <jats:italic>Tuta absoluta<\/jats:italic>\n                    (Meyrick), is an invasive tomato pest found worldwide. Sustainable control strategies aimed at increasing biological control approaches and decreasing chemical inputs are required, due to the tendency to develop insecticide resistance. In this study, the lethal and sublethal effects of four chemical insecticides (abamectin, indoxacarb, chlorantraniliprole, and spinosad) and the sublethal effects of the entomopathogenic fungus\n                    <jats:italic>Metarhizium anisopliae<\/jats:italic>\n                    (Metschnikoff) on a widespread TLM egg parasitoid,\n                    <jats:italic>Trichogramma brassicae<\/jats:italic>\n                    Bezdenko, were estimated. Concentration mortality response bioassays enabled the estimation of lethal concentrations of the tested insecticides for the parasitoids, with chlorantraniliprole having the lowest LC\n                    <jats:sub>50<\/jats:sub>\n                    and indoxacarb the highest. The LC\n                    <jats:sub>25<\/jats:sub>\n                    and LC\n                    <jats:sub>50<\/jats:sub>\n                    of the tested insecticides on the TLM were sprayed on eggs and then offered at three time intervals to the parasitoids. The fertility and other life table parameters of the individuals emerging from the treated eggs were estimated. All of the chemical insecticides, but not the fungus, had harmful effects on\n                    <jats:italic>T<\/jats:italic>\n                    .\n                    <jats:italic>brassicae<\/jats:italic>\n                    . The insecticide applications caused a 3.84\u20135.17 times reduction in the net reproductive rate (\n                    <jats:italic>R<\/jats:italic>\n                    <jats:sub>\n                      <jats:italic>0<\/jats:italic>\n                    <\/jats:sub>\n                    ) compared with the control. No parameters were affected by spraying the fungus in the 0h treatment, but effects were recorded at 24 and\/or 48h, except for the gross reproduction rate (\n                    <jats:italic>GRR<\/jats:italic>\n                    ). The value of the intrinsic rate of increase (\n                    <jats:italic>r<\/jats:italic>\n                    <jats:sub>\n                      <jats:italic>m<\/jats:italic>\n                    <\/jats:sub>\n                    ) also decreased to 0.528\u20130.617 after the insecticide treatments. The doubling time (\n                    <jats:italic>DT<\/jats:italic>\n                    ) increased in all treatments compared to the control. Nevertheless, the generation time (\n                    <jats:italic>T<\/jats:italic>\n                    ) was only very slightly affected. In addition, in the combination experiments,\n                    <jats:italic>M<\/jats:italic>\n                    .\n                    <jats:italic>anisopliae<\/jats:italic>\n                    showed a remarkable synergism with\n                    <jats:italic>T<\/jats:italic>\n                    .\n                    <jats:italic>brassicae<\/jats:italic>\n                    in controlling TLM eggs. These results indicate that low levels of lethal effects on key biological control agents should be considered in the choice of insecticides to be included in sustainable TLM control packages.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0243334","type":"journal-article","created":{"date-parts":[[2021,7,30]],"date-time":"2021-07-30T13:42:08Z","timestamp":1627652528000},"page":"e0243334","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":35,"title":["Lethal and sublethal effects of synthetic and bio-insecticides on Trichogramma brassicae parasitizing Tuta absoluta"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7709-4912","authenticated-orcid":true,"given":"Zahra","family":"Nozad-Bonab","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mir Jalil","family":"Hejazi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shahzad","family":"Iranipour","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mehdi","family":"Arzanlou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Biondi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,7,30]]},"reference":[{"key":"pone.0243334.ref001","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1146\/annurev-ento-031616-034933","article-title":"Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future","volume":"63","author":"A Biondi","year":"2018","journal-title":"Annu Rev Entomol"},{"key":"pone.0243334.ref002","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1007\/s10340-017-0867-7","article-title":"From the Western Palearctic region to beyond: Tuta absoluta 10 years after invading Europe","volume":"90","author":"MR Campos","year":"2017","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref003","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1127\/entomologia\/2018\/0749","article-title":"Occurrence, biology, natural enemies and management of Tuta absoluta in Africa","volume":"38","author":"R Mansour","year":"2018","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref004","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1007\/s10340-018-1062-1","article-title":"Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges","volume":"92","author":"P Han","year":"2018","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref005","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1127\/entomologia\/2019\/0778","article-title":"First record of Tuta absoluta in Haiti","volume":"38","author":"F Verheggen","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref006","doi-asserted-by":"crossref","first-page":"1373","DOI":"10.1007\/s10340-018-1057-y","article-title":"Global geographic distribution of Tuta absoluta as affected by climate change","volume":"92","author":"PA Santana","year":"2019","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref007","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1111\/epp.2577","article-title":"The first report and control strategies of Tuta absoluta in Iran","volume":"42","author":"V Baniameri","year":"2012","journal-title":"Bull OEPP"},{"key":"pone.0243334.ref008","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1127\/entomologia\/2019\/0685","article-title":"Elucidating key biological parameters of Tuta absoluta on different host plants and under various temperature and relative humidity regimes","volume":"39","author":"A Cherif","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref009","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1007\/s10340-019-01094-9","article-title":"Geographic variation of host preference by the invasive tomato leaf miner Tuta absoluta: implications for host range expansion","volume":"92","author":"S Sylla","year":"2019","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref010","unstructured":"Asadi amir abadi F, Asgari Sh, Rastegar Zh. Effect of microbial insecticides Bacillus thurengiensis, Beauveria bassiana, Metarhizium anisopliae on tomato leaf miner, Tuta absoluta. 21th Plant Protection Congress, Iran, Urmia, 23\u201327 Agu, 2014: 632p."},{"key":"pone.0243334.ref011","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1186\/s42269-020-00382-0","article-title":"Comparative toxicity of new insecticides generations against tomato leafminer Tuta absoluta and their biochemical effects on tomato plants","volume":"44","author":"MA-H Kandil","year":"2020","journal-title":"Bull Natl Res Cent"},{"key":"pone.0243334.ref012","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1590\/S1519-566X2005000100016","article-title":"Insecticide resistance in Argentine populations of Tuta absoluta (Lepidoptera: Gelechiidae)","volume":"34","author":"MMM Lietti","year":"2005","journal-title":"Neotrop Entomol"},{"key":"pone.0243334.ref013","doi-asserted-by":"crossref","first-page":"210","DOI":"10.3923\/ijar.2014.210.218","article-title":"Effect of certain low toxicity insecticides against tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae) with reference to their residues in harvested tomato fruits","volume":"9","author":"YA Mahmoud","year":"2014","journal-title":"Int J Agric Res"},{"key":"pone.0243334.ref014","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.pestbp.2011.10.008","article-title":"Metabolic mechanisms involved in the resistance of field populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to spinosad","volume":"102","author":"M Reyes","year":"2012","journal-title":"Pestic Biochem Phys"},{"key":"pone.0243334.ref015","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1002\/ps.3404","article-title":"Determination of baseline susceptibility of European populations of Tuta absoluta (Meyrick) to indoxacarb and chlorantraniliprole using a novel dip bioassay method","volume":"69","author":"E Roditakis","year":"2013","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref016","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1007\/s10340-015-0643-5","article-title":"First report of Tuta absoluta resistance to diamide insecticides","volume":"88","author":"E Roditakis","year":"2015","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref017","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1146\/annurev.ento.52.110405.091440","article-title":"The low lethal effects of pesticides on beneficial arthropods","volume":"52","author":"N Desneux","year":"2007","journal-title":"Annu Rev Entomol"},{"key":"pone.0243334.ref018","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1127\/entomologia\/2018\/0744","article-title":"Lethal, low lethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta","volume":"38","author":"LC Passos","year":"2018","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref019","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1007\/s10340-018-01074-5","article-title":"Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta","volume":"92","author":"MA Soares","year":"2019","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref020","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-017-13413-0","article-title":"Citrus peel essential oil nanoformulations to control the tomato borer, Tuta absoluta: chemical properties and biological activity","volume":"7","author":"O Campolo","year":"2017","journal-title":"Scientific reports"},{"key":"pone.0243334.ref021","doi-asserted-by":"crossref","first-page":"126986","DOI":"10.1016\/j.chemosphere.2020.126986","article-title":"Can contamination by major systemic insecticides affect the voracity of the harlequin ladybird?","volume":"256","author":"C Dai","year":"2020","journal-title":"Chemosphere"},{"key":"pone.0243334.ref022","article-title":"Sublethal effect of spirotetramat on the life table and population growth of Frankliniella occidentalis (Thysanoptera: Thripidae)","author":"H-Y Liang","year":"2021","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref023","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1007\/s10340-019-01086-9","article-title":"Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook","volume":"92","author":"RNC Guedes","year":"2019","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref024","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1002\/ps.2131","article-title":"Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta","volume":"67","author":"GA Silva","year":"2011","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref025","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1127\/entomologia\/2019\/0861","article-title":"Resistance against clothianidin and associated fitness costs in the chive maggot, Bradysia odoriphaga","volume":"39","author":"H Gul","year":"2019","journal-title":"Entomol. General"},{"key":"pone.0243334.ref026","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1007\/s10646-018-1954-0","article-title":"Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae)","volume":"27","author":"DA P\u00e9rez-Aguilar","year":"2018","journal-title":"Ecotoxicology"},{"key":"pone.0243334.ref027","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1127\/entomologia\/2019\/0865","article-title":"Clothianidin-induced sublethal effects and expression changes of vitellogenin and ecdysone receptors genes in the melon aphid, Aphis gossypii","volume":"39","author":"F Ullah","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref028","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1127\/entomologia\/2019\/0887","article-title":"Acetamiprid-induced hormetic effects and vitellogenin gene (Vg) expression in the melon aphid, Aphis gossypii","volume":"39","author":"F Ullah","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref029","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1127\/entomologia\/2019\/0892","article-title":"Imidacloprid-induced hormesis effects on demographic traits of the melon aphid, Aphis gossypii","volume":"39","author":"F Ullah","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref030","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1127\/entomologia\/2019\/0816","article-title":"Demographic analysis of progeny fitness and timing of resurgence of Laodelphax striatellus after insecticides exposure","volume":"39","author":"Y Zhang","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref031","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1007\/s10526-013-9525-z","article-title":"Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect","volume":"58","author":"F Garcia-del-Pino","year":"2013","journal-title":"BioControl"},{"key":"pone.0243334.ref032","first-page":"63","article-title":"Efficacy of three entomopathogenic agents for control the tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)","volume":"11","author":"HH Shalaby","year":"2013","journal-title":"Nat Sci"},{"key":"pone.0243334.ref033","first-page":"81","article-title":"Parasitic insects and mites as potential biocontrol agents for a devastative pest of tomato, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) in the world: a review","volume":"2","author":"K Ghoneim","year":"2014","journal-title":"Int J Curr Adv Res"},{"key":"pone.0243334.ref034","first-page":"52","article-title":"Predatory insects and arachnids as potential biological control agents against the invasive tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), in perspective and prospective","volume":"2","author":"K Ghoneim","year":"2014","journal-title":"J Entomol Zool"},{"key":"pone.0243334.ref035","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1080\/09670874.2014.941043","article-title":"An immunological method for granulovirus detection in larvae of Tuta absoluta: searching for isolates with prospects for biological control of this pest in Colombia","volume":"60","author":"J G\u00f3mez-Valderrama","year":"2014","journal-title":"Int J Pest Manage"},{"key":"pone.0243334.ref036","first-page":"2067","article-title":"Evaluations of three Bacillus thuringiensis against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt","volume":"3","author":"MM Sabbour","year":"2014","journal-title":"Int J Sci Res"},{"key":"pone.0243334.ref037","first-page":"72","article-title":"Natural enemies of Tuta absoluta (Lepidoptera: Gelechiidae) in Oued Righ region, an arid area of Algeria","volume":"8","author":"A Dehliz","year":"2015","journal-title":"A J Entomol"},{"key":"pone.0243334.ref038","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.biocontrol.2018.03.016","article-title":"Selection of flowering plants to enhance the biological control of Tuta absoluta using parasitoids","volume":"122","author":"J Arn\u00f3","year":"2018","journal-title":"Biol Control"},{"key":"pone.0243334.ref039","article-title":"Challenges facing arthropod biological control: identifying traits for genetic improvement of predators in protected crops","author":"P Bielza","year":"2020","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref040","doi-asserted-by":"crossref","first-page":"1467","DOI":"10.1007\/s10340-018-1025-6","article-title":"Functional response and age-specific foraging behavior of Necremnus tutae and N. cosmopterix, native natural enemies of the invasive pest Tuta absoluta in Mediterranean area","volume":"92","author":"N Bodino","year":"2019","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref041","first-page":"28","article-title":"Parasitoid complex of the tomato leaf miner, Tuta absoluta (Meyrick 1917), (Lepidoptera: Gelechiidae) in Hatay, Turkey","volume":"14","author":"M. Do\u011fanlar","year":"2011","journal-title":"J Nat Sci"},{"key":"pone.0243334.ref042","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1111\/epp.2564","article-title":"Biological control of Tuta absoluta in Argentina and Italy: evaluation of indigenous insects as natural enemies","volume":"42","author":"MG Luna","year":"2012","journal-title":"EPPO Bulletin"},{"key":"pone.0243334.ref043","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1515\/jppr-2015-0029","article-title":"Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae), a predatory species of the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Iran","volume":"55","author":"F. Sohrabi","year":"2015","journal-title":"J Plant Prot Res"},{"key":"pone.0243334.ref044","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1007\/s10340-013-0531-9","article-title":"Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies","volume":"86","author":"L Zappal\u00e0","year":"2013","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref045","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1007\/s10340-018-01078-1","article-title":"A re-examination of Tuta absoluta parasitoids in South America for optimized biological control","volume":"92","author":"NG Salas Gervassio","year":"2019","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref046","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/978-1-4615-4577-4_8","volume-title":"Nontarget Effects of Biological Control","author":"DB Orr","year":"2000"},{"key":"pone.0243334.ref047","doi-asserted-by":"crossref","first-page":"2085","DOI":"10.1603\/EC12221","article-title":"Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes","volume":"105","author":"T Cabello","year":"2012","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref048","doi-asserted-by":"crossref","first-page":"2310","DOI":"10.1603\/EC13092","article-title":"Suitability of the Pest\u2010Plant System Tuta absoluta (Lepidoptera: Gelechiidae)\u2010Tomato for Trichogramma (Hymenoptera: Trichogrammatidae) Parasitoids and Insights for Biological control","volume":"106","author":"A Chailleux","year":"2013","journal-title":"J Econ Entomol"},{"key":"pone.0243334.ref049","doi-asserted-by":"crossref","first-page":"801","DOI":"10.4001\/003.022.0410","article-title":"Assessment of Two Trichogramma Species for the Control of Tuta absoluta in North African Tomato Greenhouses","volume":"22","author":"SA El-Arnaouty","year":"2014","journal-title":"Afr Entomol"},{"key":"pone.0243334.ref050","doi-asserted-by":"crossref","first-page":"1479","DOI":"10.1007\/s10340-019-01091-y","article-title":"Relative importance of host and plant semiochemicals in the foraging behavior of Trichogramma achaeae, an egg parasitoid of Tuta absoluta","volume":"92","author":"L Gontijo","year":"2019","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref051","doi-asserted-by":"crossref","unstructured":"Parra JRP. Mass rearing of egg parasitoids for biological control programs. In: C\u00f4nsoli FL, Parr JRP, Zucchi RA, editors. Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Series: Progress of Biological Control. Vol 9. Springer Netherlands; 2010. pp. 267\u2013292.","DOI":"10.1007\/978-1-4020-9110-0_10"},{"key":"pone.0243334.ref052","first-page":"109","article-title":"Evaluation of Trichogramma brassicae native strains as egg parasitoid of tomato leafminer, Tuta absoluta (Meyrick) in the laboratory conditions","volume":"2","author":"R Ahmadipour","year":"2015","journal-title":"Bio Control in Plant Prote"},{"key":"pone.0243334.ref053","doi-asserted-by":"crossref","first-page":"112","DOI":"10.4236\/oje.2017.72009","article-title":"Assessment of two Trichogramma species with Bacillus thuringiensis var. kurstaki for the control of the tomato leafminer Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) in Iran","volume":"7","author":"Gh Alsaedi","year":"2017","journal-title":"Open J Ecol"},{"key":"pone.0243334.ref054","first-page":"2667","article-title":"Behavioral and biological effects of exposure to Tuta absoluta (Lepidoptera: Gelechiidae) Sex Pheromone on Several Trichogramma (Hymenoptera: Trichogrammatidae) Populations","volume":"111","author":"S Ahmadi","year":"2018","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref055","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1093\/jisesa\/iez040","article-title":"Effect of age-dependent parasitism in Eggs of Tuta absoluta (Lepidoptera: Gelechiidae) on intraguild predation between Nabis pseudoferus (Hemiptera: Nabidae) and Trichogramma brassicae (Hymenoptera: Trichogrammatidae)","volume":"19","author":"M Mohammadpour","year":"2019","journal-title":"J Insect Sci"},{"key":"pone.0243334.ref056","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1127\/entomologia\/2018\/0675","article-title":"Host plants of the polyphagous grapevine moth Lobesia botrana during larval stage modulate moth egg quality and subsequent parasitism by the parasitoid Trichogramma cacoeciae","volume":"38","author":"D Thi\u00e9ry","year":"2018","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref057","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1127\/entomologia\/2019\/0853","article-title":"Performance of Trichogramma pintoi when parasitizing eggs of the oriental fruit moth Grapholita molesta","volume":"39","author":"X Guo","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref058","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1127\/entomologia\/2019\/0857","article-title":"Impact of host suitability on oviposition preference toward fertilized and unfertilized host eggs in two Trichogramma parasitoid species","volume":"39","author":"X-Y Li","year":"2019","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref059","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1007\/s10340-013-0498-6","article-title":"Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta","volume":"86","author":"A Chailleux","year":"2013","journal-title":"J Pest Sci"},{"key":"pone.0243334.ref060","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0048068","article-title":"Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta","volume":"7","author":"A Chailleux","year":"2012","journal-title":"PLoS One"},{"key":"pone.0243334.ref061","first-page":"236","article-title":"Parasitism of South American tomato moth eggs by Trichogramma evanescens (Hymenoptera: Trichogrammatidae)","volume":"35","author":"R Payer","year":"2012","journal-title":"Revista de Ci\u00eancias Agr\u00e1rias"},{"key":"pone.0243334.ref062","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1016\/j.toxicon.2010.03.008","article-title":"Metarhizium anisopliae enzymes and toxins","volume":"56","author":"A Schrank","year":"2010","journal-title":"Toxicon"},{"key":"pone.0243334.ref063","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1023\/A:1010722914299","article-title":"Entomogenous fungi as promising biopesticides for tick control","volume":"24","author":"GP Kaaya","year":"2000","journal-title":"Exp Appl Acarol"},{"key":"pone.0243334.ref064","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s10493-008-9170-x","article-title":"Topically applied myco-acaricides for the controlof cattle ticks: overcoming the challenges","volume":"46","author":"P Polar","year":"2008","journal-title":"Exp Appl Acarol"},{"key":"pone.0243334.ref065","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1002\/ps.2780370410","article-title":"The entomopathogenic fungus Metarhizium anisopliae and its potential as a biocontrol agent","volume":"37","author":"G Zimmermann","year":"1993","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref066","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1603\/EC13404","article-title":"Efficacy of entomopathogenic fungus Metarhizium anisopliae against Tuta absoluta (Lepidoptera: Gelechiidae)","volume":"107","author":"J Contreras","year":"2014","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref067","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/j.funeco.2009.05.001","article-title":"Fungal entomopathogens: new insights on their ecology","volume":"2","author":"FE Vega","year":"2009","journal-title":"Fungal Ecol"},{"key":"pone.0243334.ref068","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1002\/ps.3396","article-title":"The non-target impact of spinosyns on beneficial arthropods, a review","volume":"68","author":"A Biondi","year":"2012","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref069","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0076548","article-title":"Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects?","volume":"8","author":"A Biondi","year":"2013","journal-title":"PLoS One"},{"key":"pone.0243334.ref070","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev-ento-010715-023646","article-title":"Pesticide-Induced Stress in Arthropod Pests for Optimized Integrated Pest Management Programs","volume":"61","author":"RNC Guedes","year":"2016","journal-title":"Annu Rev Entomol"},{"key":"pone.0243334.ref071","doi-asserted-by":"crossref","first-page":"2716","DOI":"10.1002\/ps.5380","article-title":"Selectivity of novel and traditional insecticides used for management of whiteflies on the parasitoid Encarsia formosa","volume":"75","author":"Z Wang","year":"2019","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref072","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1093\/jee\/tox079","article-title":"Lethal and sublethal effects of some chemical and biological insecticides on Tuta absoluta (Lepidoptera: Gelechiidae) eggs and neonates","volume":"110","author":"Z Nozad-Bonab","year":"2017","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref073","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1093\/oso\/9780195066876.001.0001","volume-title":"Applied Demography for Biologists, with Special Emphasis on Insects","author":"JR Carey","year":"1993"},{"key":"pone.0243334.ref074","first-page":"1","article-title":"Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum: with a new method to project the uncertainty of population grow th and consumption","volume":"111","author":"HW Huang","year":"2018","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref075","first-page":"102","article-title":"Age-Stage, two-sex life table: an introduction to theory, data analysis, and application","volume":"40","author":"H Chi","year":"2020","journal-title":"Entomol Gen"},{"key":"pone.0243334.ref076","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1093\/jee\/18.2.265a","article-title":"A method of computing the effectiveness of an insecticide","volume":"18","author":"W Abbott","year":"1925","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref077","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1093\/ee\/17.1.26","article-title":"Life-table analysis incorporating both sexes and variable development rate among individuals","volume":"17","author":"H Chi","year":"1988","journal-title":"Environ. Entomol"},{"key":"pone.0243334.ref078","unstructured":"Chi H. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. 2018. http:\/\/140.120.197.173\/Ecology\/ [accessed on Jan 2021]."},{"key":"pone.0243334.ref079","first-page":"225","article-title":"Two new methods for the study of insect population ecology","volume":"24","author":"H Chi","year":"1985","journal-title":"Bull. Inst. Zool Academia Sinica"},{"key":"pone.0243334.ref080","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1603\/0046-225X-35.1.10","article-title":"Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate","volume":"35","author":"H Chi","year":"2006","journal-title":"Environ Entomol"},{"key":"pone.0243334.ref081","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1002\/ps.3618","article-title":"Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table","volume":"70","author":"Shu-Jen Tuan","year":"2014","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref082","doi-asserted-by":"crossref","first-page":"1936","DOI":"10.1002\/ps.3920","article-title":"Erratum: Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table","volume":"70","author":"Shu-Jen Tuan","year":"2014","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref083","doi-asserted-by":"crossref","unstructured":"Efron B, Tibshirani RJ. An introduction to the bootstrap. 1994. CRC press.","DOI":"10.1201\/9780429246593"},{"key":"pone.0243334.ref084","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1002\/ps.1126","article-title":"Comparing ecological risks of pesticides: the utility of a Risk Quotient ranking approach across refinements of exposure","volume":"62","author":"RK Peterson","year":"2006","journal-title":"Pest Manag Sci"},{"key":"pone.0243334.ref085","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1016\/j.chemosphere.2010.04.070","article-title":"Risk assessment of insecticides used in rice on miridbug, Cyrtorhinus lividipennis Reuter, the important predator of brown planthopper, Nilaparvata lugens (Stal.)","volume":"80","author":"G Preetha","year":"2010","journal-title":"Chemosphere"},{"key":"pone.0243334.ref086","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1006\/bcon.1996.0498","article-title":"Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for Scarab Grub control","volume":"8","author":"AM Koppenh\u00f6fer","year":"1997","journal-title":"Biol Control"},{"key":"pone.0243334.ref087","doi-asserted-by":"crossref","first-page":"35","DOI":"10.17221\/82\/2015-PPS","article-title":"Synergism of entomopathogenic fungus, Metarhizium anisopliae incorporated with fipronil against oil palm pest subterranean termite, Coptotermes curvignathus","volume":"52","author":"JE Yii","year":"2016","journal-title":"Plant Prot Sci"},{"key":"pone.0243334.ref088","first-page":"713","article-title":"Parasitism of Phyllophaga hirticula (Coleoptera: Scarabaeidae) by Heterorhabditis heliothidis and Steinernema carpocapsae","volume":"58","author":"DJ Finney","year":"1964","journal-title":"J Invertebr Pathol"},{"key":"pone.0243334.ref089","first-page":"87","article-title":"Impacts of pesticides on arthropod biological control agents","volume":"2","author":"Kh Talebi","year":"2008","journal-title":"Pest Technology"},{"key":"pone.0243334.ref090","doi-asserted-by":"crossref","first-page":"01","DOI":"10.12741\/ebrasilis.v3i1.52","article-title":"Impact and selectivity of insecticides to predators and parasitoides","volume":"3","author":"FL Fernandes","year":"2010","journal-title":"EntomoBrasilis"},{"key":"pone.0243334.ref091","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1603\/0022-0493-93.3.577","article-title":"Effect of insecticides on Trichogramma exiguum (Trichogrammatidae: Hymenoptera) preimaginal development and adult survival","volume":"93","author":"ChP-C Suh","year":"2000","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref092","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.1007\/s10646-020-02235-y","article-title":"Side effects of chlorantraniliprole, phosalone and spinosad on the egg parasitoid, Trichogramma brassicae","volume":"29","author":"E Parsaeyan","year":"2020","journal-title":"Ecotoxicology"},{"key":"pone.0243334.ref093","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1603\/0022-0493-96.4.1083","article-title":"Effects of methoxyfenozide, indoxacarb, and other insecticides on the beneficial egg parasitoid Trichogramma nr. brassicae (Hymenoptera: Trichogrammatidae) under laboratory and field conditions","volume":"96","author":"S Hewa-Kapuge","year":"2003","journal-title":"J Eco Entomol"},{"key":"pone.0243334.ref094","first-page":"135","volume-title":"Introduction to Insect Pest Management","author":"F. W. Stehr","year":"1982"},{"key":"pone.0243334.ref095","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/S1049-9644(02)00117-2","article-title":"Quality assessment of three species of commercially produced Trichogramma and the first report of thelytoky in commercially produced Trichogramma","volume":"26","author":"JG Lundgren","year":"2003","journal-title":"Biol Control"},{"key":"pone.0243334.ref096","first-page":"61","article-title":"Side-Effects of indoxacarb and lufenuron on Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) under laboratory conditions","volume":"37","author":"A Afshari","year":"2014","journal-title":"Plant Prot"},{"key":"pone.0243334.ref097","first-page":"24.1","article-title":"Annual review of entomology biological control with Trichogramma in China: history, present status and perspectives","volume":"66","author":"L-Sh Zang","year":"2021","journal-title":"Annu. Rev. Entomol"},{"key":"pone.0243334.ref098","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1007\/s10526-007-9096-y","article-title":"Toxicity and kinetics of spinosad in different developmental stages of the endoparasitoid Hyposoter Didymator (Hymenoptera: Ichneumonidae) and its host Spodoptera littoralis larvae (Lepidoptera: Noctuidae)","volume":"53","author":"P Medina","year":"2008","journal-title":"BioControl"},{"key":"pone.0243334.ref099","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.biocontrol.2007.10.022","article-title":"Lethal and sublethal effects of spinosad-based GF-120 bait on the Tephritid parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae)","volume":"44","author":"L Ruiz","year":"2008","journal-title":"Biol Control"},{"key":"pone.0243334.ref100","first-page":"1","article-title":"Physiological selectivity of insecticides to Apis mellifera (Hymenoptera: Apidae) and Protonectarina sylveirae (Hymenoptera: Vespidae) in citrus","volume":"51","author":"MES Fernandes","year":"2008","journal-title":"Sociobiology"},{"key":"pone.0243334.ref101","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.biocontrol.2004.04.013","article-title":"Action of insect growth regulator insecticides and spinosad on life history parameters and absorption in third-instar larvae of the endoparasitoid Hyposoter didymator","volume":"31","author":"MI Schneider","year":"2004","journal-title":"Biol Control"},{"key":"pone.0243334.ref102","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1046\/j.1439-0418.2001.00513.x","article-title":"Selectivity of insecticides to the egg parasitoid Trichogramma galloi Zucchi, 1988, (Hym., Trichogrammatidae)","volume":"125","author":"FL C\u00f4nsoli","year":"2001","journal-title":"J Appl Entomol"},{"key":"pone.0243334.ref103","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1111\/j.1439-0418.2006.01072.x","article-title":"Non-target effects of three biorationale insecticides on two endolarval parasitoids of Liriomyza sativae (Dipt., Agromyzidae)","volume":"130","author":"MB Hossain","year":"2006","journal-title":"J Appl Entomol"},{"key":"pone.0243334.ref104","doi-asserted-by":"crossref","first-page":"362","DOI":"10.4236\/aces.2015.53038","article-title":"Effect of insecticides on Trichogramma parasitoides used in biological control against Prays oleae insect pest","volume":"5","author":"I Blibech","year":"2015","journal-title":"ACES"},{"key":"pone.0243334.ref105","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.cropro.2011.12.007","article-title":"Susceptibility of adult Trichogramma nubilale (Hymenoptera: Trichogrammatidae) to selected insecticides with different modes of action","volume":"34","author":"Y Wang","year":"2012","journal-title":"Crop Prot"},{"key":"pone.0243334.ref106","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1111\/j.1439-0418.1998.tb01459.x","article-title":"Side-effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (Lep., Gelechiidae)","volume":"122","author":"FL C\u00f4nsoli","year":"1998","journal-title":"J App Entomol"},{"key":"pone.0243334.ref107","doi-asserted-by":"crossref","first-page":"275","DOI":"10.4025\/actasciagron.v25i2.1771","article-title":"Side-effects of insecticides used in tomato fields on Trichogramma pretiosum (Hymenoptera, Trichogrammatidae)","volume":"25","author":"GA Carvalho","year":"2003","journal-title":"Acta Sci Agron"},{"key":"pone.0243334.ref108","first-page":"1117","article-title":"Toxicity of some new insecticides against Trichogramma chilonis (Hymenoptera: Trichogrammatidae) under laboratory and extended laboratory conditions","volume":"43","author":"Sattar Sh","year":"2011","journal-title":"Pak J Zool"},{"key":"pone.0243334.ref109","doi-asserted-by":"crossref","first-page":"1775","DOI":"10.1016\/S0045-6535(97)10071-6","article-title":"Sublethal effects of the insecticide chlorpyrifos on the sex pheromonal communication of Trichogramma brassicae","volume":"36","author":"J-M Delpuech","year":"1998","journal-title":"Chemosphere"},{"key":"pone.0243334.ref110","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1016\/S0045-6535(98)00310-5","article-title":"Modifications of the sex pheromonal communication of Trichogramma brassicae a sublethal dose of deltamethrin","volume":"38","author":"J-M Delpuech","year":"1999","journal-title":"Chemosphere"},{"key":"pone.0243334.ref111","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s41348-019-00280-2","article-title":"Lethal and parasitism effects of selected novel pesticides on adult Trichogramma chilonis (Hymenoptera: Trichogrammatidae)","volume":"127","author":"M Ashraf Khan","year":"2020","journal-title":"J Plant Dis Prot"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0243334","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,5]],"date-time":"2024-09-05T09:41:06Z","timestamp":1725529266000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0243334"}},"subtitle":[],"editor":[{"given":"Nicolas","family":"Desneux","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,7,30]]},"references-count":111,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7,30]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0243334","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.11.20.391003","asserted-by":"object"}]},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,30]]}}}