Submission to: Phytoparasitica Occurrence of ash whitefly, Siphoninus phillyreae (Haliday) (Hemiptera: Aleyrodidae), in Brazil

Submission to: Phytoparasitica Occurrence of ash whitefly, Siphoninus phillyreae (Haliday) (Hemiptera: Aleyrodidae), in Brazil | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Short Report Submission to: Phytoparasitica Occurrence of ash whitefly, Siphoninus phillyreae (Haliday) (Hemiptera: Aleyrodidae), in Brazil André Lourenção, Gregory A. Evans, Nyeppson de Sousa Soares, Gabriel Rodrigues Palma, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4849950/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 20 Mar, 2025 Read the published version in Phytoparasitica → Version 1 posted 13 You are reading this latest preprint version Abstract Siphoninus phillyreae (Haliday) (Hemiptera: Aleyrodidae) is a polyphagous species with a wide geographical distribution and high invasion potential. In South America, it has been documented in Venezuela, Chile, Peru and Argentina. Pomegranate leaves [ Punica granatum L. (Lythraceae)] containing whitefly eggs, nymphs, puparia, and adults were collected in the municipalities of Campinas, Piracicaba (São Paulo), Planaltina (Goiás), São João dos Patos (Maranhão), Floriano (Piauí), and Janaúba (Minas Gerais). Based on morphological characters, the species was identified as S. phillyreae in the collections. Additionally, parasitism by Encarsia brasiliensis (Hempel) was observed in Piracicaba. The adults collected in Piracicaba underwent molecular characterization, validating the morphological identification. In Brazil, the pomegranate tree is often grown as an ornamental plant in gardens due to the beauty of its leaves, flowers, fruits, and medicinal properties. Thus, due to the increase in pomegranate cultivation, an appropriate management plan for this pest is necessary. Therefore, this is the first record of the S. phillyreae in Brazil, expanding its distribution in South America. Crops Invasive species Pomegranate Punica granatum Figures Figure 1 Figure 2 Figure 3 Figure 4 Full Text Siphoninus phillyreae (Haliday) is a polyphagous and widely distributed species that has shown a great capacity to invade new habitats. This species was first described as Aleyrodes phillyreae by Haliday in 1835, collected from Phillyrea latifolia L. (Oleaceae) in Dublin, Ireland, and later as Aleyrodes dubia by Heeger in 1859, from Fraxinus sp. (Oleaceae) in Laxenburg, Germany (CABI, 2024). The genus Siphoninus was described by Silvestri in 1915, who erected S. finitimus as the type species, which is currently considered a synonym of S. phillyreae (Mound & Halsey, 1978). In addition to A. dubia and S. finitimus , A. phillyreae , Aleurochiton dubius , Aleurodes phylliceae , Asterochiton phillyreae , S. dubiosa , S. granati , and Trialeurodes inaequalis are synonyms of S. phillyreae (Evans, 2008). The high number of synonyms of S. phillyreae can be attributed to the morphological variability of its pupal case (CABI, 2024). Native to Europe, the Mediterranean, and North Africa (Nguyen & Hamon, 2020), S. phillyreae is found in numerous countries across Africa, Asia, Europe, North America, Oceania, and South America (CABI, 2024) (Fig. 1). In South America, it has been documented in Venezuela (Arnal et al., 1994), Chile (Munoz & Beéche, 1995), Argentina (Viscarret & Botto, 1997) and Peru (Valencia, 2011) (Fig. 2). As there is no reference to the presence of S. phillyreae in Brazil, this communication aims to record its occurrence in this country, based on collections from pomegranates Punica granatum L. (Lythraceae) in the state of São Paulo. In Brazil, in January 2015, a consultation was held at the Agronomic Institute of Campinas (IAC) to identify an Aleyrodidae specimen infesting pomegranate leaves in a residence located in Campinas (São Paulo). In January 2021, a notable whitefly infestation occurred in Piracicaba (São Paulo) on a single pomegranate plant in another residence. Subsequently, also in Piracicaba, between January and April 2023, whitefly-infested pomegranate leaves were collected from nine plants: three in the Santa Rita neighbourhood (22°45'13.95"S; 47°35'9.61"W), four on the “Luiz de Queiroz” campus of ESALQ/USP (22°42'48.17"S; 47°37'35.15"W), one in a restaurant garden in the city center (22°44'3.90"S; 47°39'1.72"W), and one on the sidewalk of Carlos Botelho Avenue (22°42'49"S; 47°38'13"W). In Planaltina (Goiás) (15°26'50.7"S; 47°37'18.2"W), we found leaves of pomegranate infested with whitefly in December 2023; São João dos Patos (Maranhão) (6°30'19"S; 43°42'00"W) and Floriano (Piauí) (6°47'33"S; 42°59'26"W) in January 2024, and Janaúba (Minas Gerais) (15°49'54.09"S; 43°16'20.12"W) in February 2024. (Table 1) presents the average temperature and rainfall found on whitefly infestations along different locations in Brazil. All infestations were collected in locations with average temperature higher than 20 °C and average rainfall lower than 0.60 mm. In future work, more covariates and samples will be collected to aid whitefly infestation predictions in Brazil (Table 1). Leaves from the collections at these locations were herborized, and subsequently, the pupal cases were mounted on microscopy slides following the protocols of Mound & Marullo (1996) and Hodges & Evans (2005). The genus Siphoninus is easily recognizable by its long siphon-like setae with expanded apices and operculum that only occupy the basal part of the vasiform orifice (Martin et al., 2000). Valencia (2011) provided morphological characters to distinguish S. phillyerae , found infesting ash ( F. americana ) and pomegranate ( P. granatum ) in Peru, from Siphoninus finitimus (Silvestri), a species synonymized with P. phillyreae by Mound & Halsey (1978), which he found on olives ( O. europaea ) in Peru and provided morphological characters to separate it from the former and removed it from synonymy. All specimens from these collections were compared with the characteristics given in Valencia (2011) for S. finitimus and S. phillyreae and were found to represent only S. phillyreae , representing the first record of its occurrence in Brazil (Fig. 2). Voucher specimens have been deposited as exsiccates of leaves and slides in the Museum of Entomology “Luiz de Queiroz” (MELQ) collection in Piracicaba (number ESALQENT001755-56) and the United States Natural History Museum (USNM), Smithsonian Institute, Aleyrodidae collection located in Beltsville, Maryland, USA (20705). Infestation levels varied in the plants inspected in Piracicaba, depending on the observation time. Leaves with a high infestation of nymphs and adults (Fig. 3a-f) displayed wavy edges, and over time, the yellowing process initiated (Fig. 3g). Additionally, leaf fall from the branches of plants highly infested with S. phillyreae was observed . In other regions of Brazil where pomegranate leaves were collected only once (Goiás, Maranhão, Minas Gerais and Piauí). In Piracicaba, 89 specimens of Encarsia Foerster (Hymenoptera: Aphelinidae) parasitoids were collected from nymphs of S. phillyreae . Morphological identification, performed using the keys of Polaszek et al. (1992, 2004), confirmed all specimens as Encarsia brasiliensis (Hempel) (formerly Encarsia hispida De Santis) (Fig. 4). Molecular characterization of these parasitoids and their hosts was conducted. Genomic DNA extraction from the specimens we identified as E. brasiliensis and S. phillyreae followed the non-destructive extraction method adapted for microhymenopteran extraction (Wengrat et al., 2021). Two fragments of the mitochondrial gene (mtDNA ) cytochrome c oxidase subunit I (COI) and the D2 expansion region of the 28S rDNA gene (28S-D2) were sequenced for the parasitoids and a COI fragment was sequenced for the whitefly. COI was amplified using the primers LCO 1490/HCO 2198 (Folmer et al., 1994) for parasitoids and whiteflies; also, for parasitoids, was amplified with primers C1-J-2183/TL2-N-3014 (Simon et al., 1994), as well as the 28S-D2 region with primers D2F/D2R (Campbell et al., 1993). PCR conditions for amplification of the COI and 28S-D2 fragments were as described in Gariepy et al. (2014), with modifications to the annealing temperatures: 50 ºC for the LCO-HCO, 51 ºC for 2183-3014, and 55 ºC for D2F and D2R. Amplicons were visualized under ultraviolet light after 1.5% agarose gel electrophoresis stained with SYBR Safe. PCR products were purified and sequenced by the Sanger method at the Agricultural Biotechnology Laboratory (CEBTEC). Sequences were deposited at GenBank under the accession numbers OR807273-OR807275 (LCO/HCO), OR807264-OR807268 (2183/3014), and OR807261-OR807263 (28S) for E. brasiliensis and PP153921-PP153925 (LCO/HCO) for S. phillyreae . After the DNA extraction, parasitoid specimens preserved in ethanol 75% were mounted on slides following the methodology of Huber (2015). Voucher specimens were deposited at the “Oscar Monte” Entomophagous Insect Collection (IB-CBE) at the Instituto Biológico, Campinas, Brazil, under the unique identifiers IB-CBE 001871 to IB-CBE 001875. This represents the second record of E. brasiliensis as a parasitoid for S. phillyreae , since Valencia (2011) also reported it from Peru, as E. hispida . Encarsia hispida was synonymized with E. brasiliensis by Polaszek et al. (2004). This is an example with strong reasons for a reversal of precedence, as discussed by Polaszek et al. (2004); however, their publication was the last official act on the taxonomy of the species. Encarsia brasiliensis has already been reported in the Brazilian states of São Paulo (Hempel, 1904; Polaszek et al., 2004), Minas Gerais (Polaszek et al., 2004; Torres et al., 2014), Bahia (Lourenção et al., 2007), Distrito Federal (Oliveira et al., 2003), Paraíba (Oliveira et al., 2019), and Maranhão (Dias-Pini et al., 2020) parasitizing Bemisia tabaci (Gennadius), Trialeurodes variabilis (Quaintance), and Aleurodicus cocois (Curtis); therefore, it likely has a wide distribution in the country. In Brazil, the pomegranate tree is often grown as an ornamental plant in gardens due to the beauty of its leaves, flowers, fruits, and medicinal properties (Bonome & Tomazi, 2022). Considering the potential spread of S. phillyreae in pomegranate cultivation areas and other crops attacked by this whitefly, evaluating the efficiency of Aleyrodidae parasitoids in Brazil is essential for its control. Most known species have been reported to parasitize B. tabaci (Oliveira et al., 2003; Lourenção et al., 2014; Torres et al., 2014; Oliveira et al., 2019). Notably, E. inaron , responsible for the reduction of S. phillyreae populations in the USA, is present in São Paulo, Minas Gerais, and the Federal District (Oliveira et al., 2003; Lourenção et al., 2014; Torres et al., 2014). Thus, in addition to the presence of E. inaron in Brazil, which is a proven efficient biological control agent of S. phillyreae , there is evidence of natural parasitism by E. brasiliensis , as observed in this study. The combined presence of E. inaron and E. brasiliensis could contribute to the sustainable control of this whitefly pest. Declarations Conflict of interest The authors declare that they have no competing interests. Author Contribution A.L.L., G.E, N.S.S, V.A.C, A.P.G.S.W., and M.S. planned and wrote the manuscript. G.E. made the whitefly identifications. V.A.C. and A.P.G.S.W. made the Encarsia identifications. A.P.G.S.W. made the molecular analysis. M.S., N.S.S., V.A.C., and G.A.E. made the map and plates. G.R.P. made the descriptive statistics and reviewed the manuscript. All authors approved the manuscript. Acknowledgement This study was supported by the Graduate Program in Entomology USP/ESALQ. We thank the National Council for Scientific and Technological Development (CNPq) for the Research Fellowship Proc. 304323/2022–5 to ALL. VAC thanks the National Institute of Science and Technology of Hymenoptera Parasitoids (INCT Hympar; CNPq Process 465562/2014-0) and the São Paulo Research Foundation (FAPESP, Process 2019/10533-2) for financial support. APGSW thanks to CNPq (grant 152666/2022-2). NSS was supported by the Coordination for the Improvement of Higher Education Personnel Brazil (CAPES – Finance Code – 001). The authors are also grateful to the Laboratory of Molecular Ecology of Arthropods and Prof. Dr. Alberto S. Corrêa (USP/ESALQ) for support in molecular extractions. The authors are grateful to the Gabriela Corrêa Morais, and Francisco Dias Morais for collecting samples of S. phillyreae in the state of Maranhão. This publication was authorized by the Brazilian Ministry of Agriculture, Cattle and Food Supply - MAPA (document no. 21000.016879/2023-86/DSV/SDA/MAPA). References Arnal, E., & Pacheco, W. (1994). Detection of the pomegranate whitefly Siphoninus phillyreae (Haliday) (Homoptera: Aleyrodidae). Boletín de Entomología Venezolana , 9(2), 199–201. Bonome, L. T. S., & Tomazi, Y. (2022). Aspectos econômicos da cultura da romãzeira. In: Lima, C.S.M., Rosa, G.G., Bonome, L.T.S (Eds.) Aspectos técnicos da cultura da romãzeira , UFFS Editora, Chapecó, pp. 7–15. 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(Hemiptera: Aleyrodidae) Biotype B in Brazil. Neotropical Entomology , 43(2), 189–191. https://doi.org/10.1007/s13744-013-0188-3 Valencia, L. V. (2011). Reestablecimiento de Siphoninus finitimus Silvestri (Hemiptera: Aleyrodidae) como una especie valida, en base a datos morfológicos, plantas hospederas y parasitoides en el Perú. Revista Peruana de Entomología , 46(2), 59–67. Viscarret, M.M., & Botto, E.N. (1997). Presencia de Siphoninus phillyreae ,"la mosca blanca de los fresnos" (Homoptera: Aleyrodidae) en la Argentina. Revista de la Sociedad Entomologica Argentina 56, 1–4. Wengrat, A. P. G. S, Coelho Junior, A., Parra, J. R. P., Takahashi, T. A., Foerster, L. A., Corrêa, A. S., Polaszek, A., Johnson, N. F., Costa, V. A., Zucchi, R. A. (2021). Integrative taxonomy and phylogeography of Telenomus remus (Scelionidae), with the first record of natural parasitism of Spodoptera spp. in Brazil. Scientific Reports , 11, 1–9. https://doi.org/10.1038/s41598-021-93510-3 Table 1 Table 1. Average temperature, rainfall, and sample size for ash whitefly, Siphoninus phillyreae infesting pomegranate leaves in Brazil (2023-2024). Location Samples Average temperature Average rainfall Piracicaba - SP 4.00 23.60 0.03 Planaltina - GO 1.00 21.30 0.34 Floriano - PI 1.00 26.90 0.9 São João dos Patos - MA 1.00 28.50 0.00 Janaúba - MG 1.00 24.40 0.53 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 20 Mar, 2025 Read the published version in Phytoparasitica → Version 1 posted Editorial decision: Accepted 17 Feb, 2025 Reviews received at journal 15 Feb, 2025 Reviewers agreed at journal 10 Feb, 2025 Reviewers agreed at journal 10 Feb, 2025 Reviews received at journal 01 Jan, 2025 Reviewers agreed at journal 09 Dec, 2024 Reviewers agreed at journal 07 Nov, 2024 Reviews received at journal 01 Sep, 2024 Reviewers agreed at journal 12 Aug, 2024 Reviewers invited by journal 09 Aug, 2024 Editor assigned by journal 06 Aug, 2024 Submission checks completed at journal 05 Aug, 2024 First submitted to journal 02 Aug, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4849950","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Short Report","associatedPublications":[],"authors":[{"id":347726639,"identity":"73a4bf27-0173-4326-8bab-d44b54ea7f1e","order_by":0,"name":"André Lourenção","email":"","orcid":"","institution":"University of São Paulo (ESALQ/USP)","correspondingAuthor":false,"prefix":"","firstName":"André","middleName":"","lastName":"Lourenção","suffix":""},{"id":347726640,"identity":"8320d3bb-5ed5-480e-b458-2a4cad9f7086","order_by":1,"name":"Gregory A. Evans","email":"","orcid":"","institution":"National Scale Insect Identifier, USDA/APHIS","correspondingAuthor":false,"prefix":"","firstName":"Gregory","middleName":"A.","lastName":"Evans","suffix":""},{"id":347726641,"identity":"d6838355-e822-4584-966d-ff8e1c3617ba","order_by":2,"name":"Nyeppson de Sousa Soares","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAsUlEQVRIiWNgGAWjYDADfhDB2ECKFskGkrUYHCBWi7lE8rHHBX9s8oxvpD97wLjjHmEtljPS0o1ntqUVm93IMTdgPFNMhHtu5JhJ8zYcTtx2I4dNgrEtgRgt+d+kef4cTtw8I/0ZsVpy2KR52A4nbpBIMCNSy5ln5iC/JM4488bcIPEMMVqOJz8DhVhifzswxD7uIEILg0ACGzOUycZAjAZgQjmApGUUjIJRMApGATYAAJmcO9mk5aMhAAAAAElFTkSuQmCC","orcid":"","institution":"University of São Paulo (ESALQ/USP)","correspondingAuthor":true,"prefix":"","firstName":"Nyeppson","middleName":"de Sousa","lastName":"Soares","suffix":""},{"id":347726643,"identity":"45437ede-1a48-40d0-bd86-e18fa487db0b","order_by":3,"name":"Gabriel Rodrigues Palma","email":"","orcid":"","institution":"Maynooth University","correspondingAuthor":false,"prefix":"","firstName":"Gabriel","middleName":"Rodrigues","lastName":"Palma","suffix":""},{"id":347726644,"identity":"113a5350-ac30-409a-a300-cde6708efd40","order_by":4,"name":"Valmir Antonio Costa","email":"","orcid":"","institution":"São Paulo’s Agency for Agribusiness Technology – IB-APTA","correspondingAuthor":false,"prefix":"","firstName":"Valmir","middleName":"Antonio","lastName":"Costa","suffix":""},{"id":347726645,"identity":"576dfd7d-9452-4d0a-8ae1-c6517762675a","order_by":5,"name":"Ana Paula Gonçalves da Silva Wengrat","email":"","orcid":"","institution":"University of São Paulo (ESALQ/USP)","correspondingAuthor":false,"prefix":"","firstName":"Ana","middleName":"Paula Gonçalves da Silva","lastName":"Wengrat","suffix":""},{"id":347726648,"identity":"c113ca68-65c3-4f18-9222-cfb37f738fd4","order_by":6,"name":"Marcoandre Savaris","email":"","orcid":"","institution":"University of São Paulo (ESALQ/USP)","correspondingAuthor":false,"prefix":"","firstName":"Marcoandre","middleName":"","lastName":"Savaris","suffix":""}],"badges":[],"createdAt":"2024-08-02 17:35:35","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4849950/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4849950/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s12600-025-01255-w","type":"published","date":"2025-03-20T15:58:06+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":63787199,"identity":"0a902537-8700-41ff-9d53-2badf1339ea6","added_by":"auto","created_at":"2024-09-02 10:48:54","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":52782,"visible":true,"origin":"","legend":"\u003cp\u003eGeographic distribution of \u003cem\u003eSiphoninus phillyreae\u003c/em\u003e (Haliday) (Hemiptera: Aleyrodidae) (CABI 2024).\u003c/p\u003e","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4849950/v1/0b7d39245ddf9b78a8bdd3b3.jpg"},{"id":63788031,"identity":"ea63fbe5-a6a0-42ce-941d-f15fc12e3a7d","added_by":"auto","created_at":"2024-09-02 10:56:54","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":50957,"visible":true,"origin":"","legend":"\u003cp\u003eCurrent distribution map of \u003cem\u003eSiphoninus phillyreae\u003c/em\u003e (Haliday) in South America (Argentina, Chile, Peru, Venezuela), including Brazil (Campinas and Piracicaba – São Paulo; Planaltina – Goiás; São João dos Patos – Maranhão; Floriano – Piauí and Janaúba – Minas Gerais).\u003c/p\u003e","description":"","filename":"2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4849950/v1/b409799a1d9b8fc140ddb521.jpg"},{"id":63787196,"identity":"4ba69655-6dfd-4677-9c21-56f46bc3415c","added_by":"auto","created_at":"2024-09-02 10:48:54","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":619672,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cem\u003eSiphoninus phillyreae \u003c/em\u003e(Haliday) adults and nymphs. (a-d) nymphs; (e) adult emergence; (f) adults and nymphs; (g) infested leaves and damage, red arrow indicating initial infestation – adult and eggs. Scale bar: 0.5 mm.\u003c/p\u003e","description":"","filename":"3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4849950/v1/349fd8e276f1fe04f0ec7a7b.jpg"},{"id":63787198,"identity":"9de68e97-9837-4f8a-93b1-1d4b9bc28119","added_by":"auto","created_at":"2024-09-02 10:48:54","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":35662,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cem\u003eEncarsia brasiliensis \u003c/em\u003e(Hempel); female. Scale bar: 0.5 mm.\u003c/p\u003e","description":"","filename":"4.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4849950/v1/780ed1831146f37aff213da1.jpg"},{"id":79121262,"identity":"0158dcb0-29ce-475a-896c-51659ad5669c","added_by":"auto","created_at":"2025-03-24 16:11:48","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1241785,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4849950/v1/d0b2cb56-efb6-42ee-87b7-877ec889d715.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Submission to: Phytoparasitica Occurrence of ash whitefly, Siphoninus phillyreae (Haliday) (Hemiptera: Aleyrodidae), in Brazil","fulltext":[{"header":"Full Text","content":"\u003cp\u003e\u003cem\u003eSiphoninus phillyreae\u003c/em\u003e (Haliday) is a polyphagous and widely distributed species that has shown a great capacity to invade new habitats. This species was first described as \u003cem\u003eAleyrodes phillyreae\u003c/em\u003e by Haliday in 1835, collected from \u003cem\u003ePhillyrea latifolia\u003c/em\u003e L. (Oleaceae) in Dublin, Ireland, and later as \u003cem\u003eAleyrodes dubia\u003c/em\u003e by Heeger in 1859, from \u003cem\u003eFraxinus\u003c/em\u003e sp. (Oleaceae) in Laxenburg, Germany (CABI, 2024). The genus \u003cem\u003eSiphoninus\u003c/em\u003e was described by Silvestri in 1915, who erected \u003cem\u003eS. finitimus\u003c/em\u003e as the type species, which is currently considered a synonym of \u003cem\u003eS.\u003c/em\u003e \u003cem\u003ephillyreae\u003c/em\u003e (Mound \u0026amp; Halsey, 1978). In addition to \u003cem\u003eA. dubia\u003c/em\u003e and \u003cem\u003eS. finitimus\u003c/em\u003e, \u003cem\u003eA. phillyreae\u003c/em\u003e,\u003cem\u003e\u0026nbsp;Aleurochiton dubius\u003c/em\u003e, \u003cem\u003eAleurodes phylliceae\u003c/em\u003e, \u003cem\u003eAsterochiton phillyreae\u003c/em\u003e, \u003cem\u003eS. dubiosa\u003c/em\u003e, \u003cem\u003eS. granati\u003c/em\u003e, and \u003cem\u003eTrialeurodes inaequalis\u003c/em\u003e are synonyms of \u003cem\u003eS. phillyreae\u003c/em\u003e (Evans, 2008). The high number of synonyms of \u003cem\u003eS. phillyreae\u003c/em\u003e can be attributed to the morphological variability of its pupal case (CABI, 2024). \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eNative to Europe, the Mediterranean, and North Africa (Nguyen \u0026amp; Hamon, 2020), \u003cem\u003eS. phillyreae\u003c/em\u003e is found in numerous countries across Africa, Asia, Europe, North America, Oceania, and South America (CABI, 2024) (Fig. 1). In South America, it has been documented in Venezuela (Arnal et al., 1994), Chile (Munoz \u0026amp; Be\u0026eacute;che, 1995), Argentina (Viscarret \u0026amp; Botto, 1997) and Peru (Valencia, 2011) (Fig. 2). As there is no reference to the presence of \u003cem\u003eS.\u003c/em\u003e \u003cem\u003ephillyreae\u003c/em\u003e in Brazil, this communication aims to record its occurrence in this country, based on collections from pomegranates \u003cem\u003ePunica granatum\u003c/em\u003e L. (Lythraceae) in the state of S\u0026atilde;o Paulo. \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eIn Brazil, in January 2015, a consultation was held at the Agronomic Institute of Campinas (IAC) to identify an Aleyrodidae specimen infesting pomegranate leaves in a residence located in Campinas (S\u0026atilde;o Paulo). In January 2021, a notable whitefly infestation occurred in Piracicaba (S\u0026atilde;o Paulo) on a single pomegranate plant in another residence. Subsequently, also in Piracicaba, between January and April 2023, whitefly-infested pomegranate leaves were collected from nine plants: three in the Santa Rita neighbourhood (22\u0026deg;45\u0026apos;13.95\u0026quot;S; 47\u0026deg;35\u0026apos;9.61\u0026quot;W), four on the \u0026ldquo;Luiz de Queiroz\u0026rdquo; campus of ESALQ/USP (22\u0026deg;42\u0026apos;48.17\u0026quot;S; 47\u0026deg;37\u0026apos;35.15\u0026quot;W), one in a restaurant garden in the city center (22\u0026deg;44\u0026apos;3.90\u0026quot;S; 47\u0026deg;39\u0026apos;1.72\u0026quot;W), and one on the sidewalk of Carlos Botelho Avenue (22\u0026deg;42\u0026apos;49\u0026quot;S; 47\u0026deg;38\u0026apos;13\u0026quot;W). In Planaltina (Goi\u0026aacute;s) (15\u0026deg;26\u0026apos;50.7\u0026quot;S; 47\u0026deg;37\u0026apos;18.2\u0026quot;W), we found leaves of pomegranate infested with whitefly in December 2023; S\u0026atilde;o Jo\u0026atilde;o dos Patos (Maranh\u0026atilde;o) (6\u0026deg;30\u0026apos;19\u0026quot;S; 43\u0026deg;42\u0026apos;00\u0026quot;W) and Floriano (Piau\u0026iacute;) (6\u0026deg;47\u0026apos;33\u0026quot;S; 42\u0026deg;59\u0026apos;26\u0026quot;W) in January 2024, and Jana\u0026uacute;ba (Minas Gerais) (15\u0026deg;49\u0026apos;54.09\u0026quot;S; 43\u0026deg;16\u0026apos;20.12\u0026quot;W) in February 2024. (Table 1) presents the average temperature and rainfall found on whitefly infestations along different locations in Brazil. All infestations were collected in locations with average temperature higher than 20 \u0026deg;C and average rainfall lower than 0.60 mm. In future work, more covariates and samples will be collected to aid whitefly infestation predictions in Brazil (Table 1). \u0026nbsp; \u0026nbsp; \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eLeaves from the collections at these locations were herborized, and subsequently, the pupal cases were mounted on microscopy slides following the protocols of Mound \u0026amp; Marullo (1996) and Hodges \u0026amp; Evans (2005). The genus \u003cem\u003eSiphoninus\u003c/em\u003e is easily recognizable by its long siphon-like setae with expanded apices and operculum that only occupy the basal part of the vasiform orifice (Martin et al., 2000). Valencia (2011) provided morphological characters to distinguish \u003cem\u003eS. phillyerae\u003c/em\u003e, found infesting ash (\u003cem\u003eF. americana\u003c/em\u003e) and pomegranate (\u003cem\u003eP. granatum\u003c/em\u003e) in Peru, from \u003cem\u003eSiphoninus finitimus\u003c/em\u003e (Silvestri), a species synonymized with \u003cem\u003eP. phillyreae\u003c/em\u003e by Mound \u0026amp; Halsey (1978), which he found on olives (\u003cem\u003eO. europaea\u003c/em\u003e) in Peru and provided morphological characters to separate it from the former and removed it from synonymy. All specimens from these collections were compared with the characteristics given in Valencia (2011) for \u003cem\u003eS. finitimus\u003c/em\u003e and \u003cem\u003eS. phillyreae\u003c/em\u003e and were found to represent only \u003cem\u003eS. phillyreae\u003c/em\u003e, representing the first record of its occurrence in Brazil (Fig. 2). Voucher specimens have been deposited as exsiccates of leaves and slides in the Museum of Entomology \u0026ldquo;Luiz de Queiroz\u0026rdquo; (MELQ) collection in Piracicaba (number ESALQENT001755-56) and the United States Natural History Museum (USNM), Smithsonian Institute, Aleyrodidae collection located in Beltsville, Maryland, USA (20705). \u0026nbsp; \u0026nbsp;\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eInfestation levels varied in the plants inspected in Piracicaba, depending on the observation time. Leaves with a high infestation of nymphs and adults (Fig. 3a-f) displayed wavy edges, and over time, the yellowing process initiated (Fig. 3g). Additionally, leaf fall from the branches of plants highly infested with \u003cem\u003eS. phillyreae\u003c/em\u003e was observed\u003cem\u003e.\u003c/em\u003e In other regions of Brazil where pomegranate leaves were collected only once (Goi\u0026aacute;s, Maranh\u0026atilde;o, Minas Gerais and Piau\u0026iacute;). \u0026nbsp; \u0026nbsp; \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eIn Piracicaba, 89 specimens of \u003cem\u003eEncarsia\u0026nbsp;\u003c/em\u003eFoerster (Hymenoptera: Aphelinidae) parasitoids were collected from nymphs of \u003cem\u003eS. phillyreae\u003c/em\u003e. Morphological identification, performed using the keys of Polaszek et al. (1992, 2004), confirmed all specimens as \u003cem\u003eEncarsia brasiliensis\u003c/em\u003e (Hempel) (formerly \u003cem\u003eEncarsia hispida\u003c/em\u003e De Santis) (Fig. 4). Molecular characterization of these parasitoids and their hosts was conducted. Genomic DNA extraction from the specimens we identified as \u003cem\u003eE. brasiliensis\u003c/em\u003e and \u003cem\u003eS.\u0026nbsp;phillyreae\u0026nbsp;\u003c/em\u003efollowed the non-destructive extraction method adapted for microhymenopteran extraction (Wengrat et al., 2021). \u0026nbsp;\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eTwo fragments of the mitochondrial gene (mtDNA\u003cem\u003e) cytochrome c oxidase subunit I\u003c/em\u003e (COI) and the D2 expansion region of the 28S rDNA gene (28S-D2) were sequenced for the parasitoids and a COI fragment was sequenced for the whitefly. COI was amplified using the primers LCO 1490/HCO 2198 (Folmer et al., 1994) for parasitoids and whiteflies; also, for parasitoids, was amplified with primers C1-J-2183/TL2-N-3014 (Simon et al., 1994), as well as the 28S-D2 region with primers D2F/D2R (Campbell et al., 1993). PCR conditions for amplification of the COI and 28S-D2 fragments were as described in Gariepy et al. (2014), with modifications to the annealing temperatures: 50 \u0026ordm;C for the LCO-HCO, 51 \u0026ordm;C for 2183-3014, and 55 \u0026ordm;C for D2F and D2R. Amplicons were visualized under ultraviolet light after 1.5% agarose gel electrophoresis stained with SYBR Safe. PCR products were purified and sequenced by the Sanger method at the Agricultural Biotechnology Laboratory (CEBTEC). \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eSequences were deposited at GenBank under the accession numbers OR807273-OR807275 (LCO/HCO), OR807264-OR807268 (2183/3014), and OR807261-OR807263 (28S) for \u003cem\u003eE. brasiliensis\u003c/em\u003e and PP153921-PP153925 (LCO/HCO) for \u003cem\u003eS. phillyreae\u003c/em\u003e.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eAfter the DNA extraction, parasitoid specimens preserved in ethanol 75% were mounted on slides following the methodology of Huber (2015). Voucher specimens were deposited at the \u0026ldquo;Oscar Monte\u0026rdquo; Entomophagous Insect Collection (IB-CBE) at the Instituto Biol\u0026oacute;gico, Campinas, Brazil, under the unique identifiers IB-CBE 001871 to IB-CBE 001875.\u003c/p\u003e\n\u003cp\u003eThis represents the second record of \u003cem\u003eE.\u0026nbsp;\u003c/em\u003e\u003cem\u003ebrasiliensis\u003c/em\u003e as a parasitoid for \u003cem\u003eS. phillyreae\u003c/em\u003e,\u003cem\u003e\u0026nbsp;\u003c/em\u003esince Valencia (2011) also reported it from Peru, as\u003cem\u003e\u0026nbsp;E. hispida\u003c/em\u003e. \u003cem\u003eEncarsia hispida\u003c/em\u003e was synonymized with \u003cem\u003eE. brasiliensis\u003c/em\u003e by Polaszek et al. (2004).\u0026nbsp;This is an example with strong reasons for a reversal of precedence, as discussed by Polaszek et al. (2004); however, their publication was the\u0026nbsp;last official act on the taxonomy of the species. \u003cem\u003eEncarsia brasiliensis\u003c/em\u003e has already been reported in the Brazilian states of S\u0026atilde;o Paulo (Hempel, 1904; Polaszek et al., 2004), Minas Gerais (Polaszek et al., 2004; Torres et al., 2014), Bahia (Louren\u0026ccedil;\u0026atilde;o et al., 2007), Distrito Federal (Oliveira et al., 2003), Para\u0026iacute;ba (Oliveira et al., 2019), and Maranh\u0026atilde;o (Dias-Pini et al., 2020) parasitizing \u003cem\u003eBemisia tabaci\u003c/em\u003e (Gennadius), \u003cem\u003eTrialeurodes variabilis\u003c/em\u003e (Quaintance), and \u003cem\u003eAleurodicus cocois\u003c/em\u003e (Curtis); therefore, it likely has a wide distribution in the country. \u0026nbsp; \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eIn Brazil, the pomegranate tree is often grown as an ornamental plant in gardens due to the beauty of its leaves, flowers, fruits, and medicinal properties (Bonome \u0026amp; Tomazi, 2022). \u0026nbsp;\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eConsidering the potential spread of \u003cem\u003eS. phillyreae\u003c/em\u003e in pomegranate cultivation areas and other crops attacked by this whitefly, evaluating the efficiency of Aleyrodidae parasitoids in Brazil is essential for its control. Most known species have been reported to parasitize \u003cem\u003eB. tabaci\u003c/em\u003e (Oliveira et al., 2003; Louren\u0026ccedil;\u0026atilde;o et al., 2014; Torres et al., 2014; Oliveira et al., 2019). Notably, \u003cem\u003eE. inaron\u003c/em\u003e, responsible for the reduction of \u003cem\u003eS. phillyreae\u003c/em\u003e populations in the USA, is present in S\u0026atilde;o Paulo, Minas Gerais, and the Federal District (Oliveira et al., 2003; Louren\u0026ccedil;\u0026atilde;o et al., 2014; Torres et al., 2014). Thus, in addition to the presence of \u003cem\u003eE. inaron\u003c/em\u003e in Brazil, which is a proven efficient biological control agent of \u003cem\u003eS.\u003c/em\u003e\u003cem\u003ephillyreae\u003c/em\u003e, there is evidence of natural parasitism by \u003cem\u003eE. brasiliensis\u003c/em\u003e, as observed in this study. The combined presence of \u003cem\u003eE.\u003c/em\u003e\u003cem\u003einaron\u003c/em\u003e and \u003cem\u003eE. brasiliensis\u003c/em\u003e could contribute to the sustainable control of this whitefly pest. \u0026nbsp;\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e \u003ch2\u003eConflict of interest\u003c/h2\u003e \u003cp\u003eThe authors declare that they have no competing interests.\u003c/p\u003e \u003c/p\u003e\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eA.L.L., G.E, N.S.S, V.A.C, A.P.G.S.W., and M.S. planned and wrote the manuscript. G.E. made the whitefly identifications. V.A.C. and A.P.G.S.W. made the Encarsia identifications. A.P.G.S.W. made the molecular analysis. M.S., N.S.S., V.A.C., and G.A.E. made the map and plates. G.R.P. made the descriptive statistics and reviewed the manuscript. All authors approved the manuscript.\u003c/p\u003e\u003ch2\u003eAcknowledgement\u003c/h2\u003e\u003cp\u003eThis study was supported by the Graduate Program in Entomology USP/ESALQ. We thank the National Council for Scientific and Technological Development (CNPq) for the Research Fellowship Proc. 304323/2022\u0026ndash;5 to ALL. VAC thanks the National Institute of Science and Technology of Hymenoptera Parasitoids (INCT Hympar; CNPq Process 465562/2014-0) and the S\u0026atilde;o Paulo Research Foundation (FAPESP, Process 2019/10533-2) for financial support. APGSW thanks to CNPq (grant 152666/2022-2). NSS was supported by the Coordination for the Improvement of Higher Education Personnel Brazil (CAPES \u0026ndash; Finance Code \u0026ndash; 001). The authors are also grateful to the Laboratory of Molecular Ecology of Arthropods and Prof. Dr. Alberto S. Corr\u0026ecirc;a (USP/ESALQ) for support in molecular extractions. The authors are grateful to the Gabriela Corr\u0026ecirc;a Morais, and Francisco Dias Morais for collecting samples of S. phillyreae in the state of Maranh\u0026atilde;o. This publication was authorized by the Brazilian Ministry of Agriculture, Cattle and Food Supply - MAPA (document no. 21000.016879/2023-86/DSV/SDA/MAPA).\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eArnal, E., \u0026amp; Pacheco, W. (1994). Detection of the pomegranate whitefly \u003cem\u003eSiphoninus phillyreae\u003c/em\u003e (Haliday) (Homoptera: Aleyrodidae). \u003cem\u003eBolet\u0026iacute;n de Entomolog\u0026iacute;a Venezolana\u003c/em\u003e, 9(2), 199\u0026ndash;201. \u003c/li\u003e\n\u003cli\u003eBonome, L. T. S., \u0026amp; Tomazi, Y. (2022). Aspectos econ\u0026ocirc;micos da cultura da rom\u0026atilde;zeira. In: Lima, C.S.M., Rosa, G.G., Bonome, L.T.S (Eds.) \u003cem\u003eAspectos t\u0026eacute;cnicos da cultura da rom\u0026atilde;zeira\u003c/em\u003e, UFFS Editora, Chapec\u0026oacute;, pp. 7\u0026ndash;15. \u003c/li\u003e\n\u003cli\u003eCABI. (2024). Datasheet Report for \u003cem\u003eSiphoninus phillyreae\u003c/em\u003e. Available at: https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.51036. Accessed: 20 February 2024. \u003c/li\u003e\n\u003cli\u003eCampbell, B., Steffen-Campbell, J. D., \u0026amp; Werren, J. H. (1993). Phylogeny of the\u003cem\u003e Nasonia\u003c/em\u003e species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer ITS2 and 28S-rDNA sequences. \u003cem\u003eInsect Molecular Biology\u003c/em\u003e, 2(4), 225\u0026ndash;237. https://doi.org/10.1111/j.1365-2583.1994.tb00142.x\u003c/li\u003e\n\u003cli\u003eDias-Pini, N. S., Monteiro, N. V., Saraiva, W. V. A., Souza, A. G. L., Santos, T. C., Zocolo, G. J., Innecco, R., \u0026amp; Silva, C. S. B. (2020 Octuber). Seletividade da mistura de \u0026oacute;leos essenciais a parasitoides de ninfas de \u003cem\u003eAleurodicus cocois\u003c/em\u003e em cajueiro. Fortaleza, Embrapa, 16p. (Boletim de Pesquisa e Desenvolvimento, 209). https://ainfo.cnptia.embrapa.br/digital/bitstream/item/217423/1/BP-209.pdf \u003c/li\u003e\n\u003cli\u003eEvans, G. A. (2008). The whiteflies (Hemiptera: Aleyrodidae) of the world and their host plants and natural enemies. Beltsville: USDA/APHIS, 703 p. Available at: https://sel.barc.usda.gov:8080/1WF/World-WhiteflyCatalog.pdf.2008. Accessed: 20 February 2024. \u003c/li\u003e\n\u003cli\u003eFolmer, O., Black, M., Hoeh, W., Lutz, R., \u0026amp; Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. \u003cem\u003eMolecular Marine Biology and Biotechnology\u003c/em\u003e, 3(5), 294\u0026ndash;299. \u003c/li\u003e\n\u003cli\u003eGariepy, T. D., Haye, T., \u0026amp; Zhang, J. (2014). A molecular diagnostic tool for the preliminary assessment of the host-parasitoid associations in biological control programmers for a new invasive pest. \u003cem\u003eMolecular Ecology\u003c/em\u003e, 23(15), 3912\u0026ndash;3924. https://doi.org/10.1111/mec.12515\u003c/li\u003e\n\u003cli\u003eHaliday, A. H. (1835). \u003cem\u003eAleyrodes phillyreae\u003c/em\u003e. \u003cem\u003eEntomological Magazine\u003c/em\u003e, 2, 119\u0026ndash;120. \u003c/li\u003e\n\u003cli\u003eHeeger, E. (1859). Beitrage zur Naturgeschichte der Insecten. Naturgeschichte der \u003cem\u003eAleyrodes dubia\u003c/em\u003e Stephens. Sitzungberichte der Kaiserlichen Akademie der Wissenschaften. \u003cem\u003eMathematische-naturwissenschaftliche klasse\u003c/em\u003e, 24, 223\u0026ndash;226.\u003c/li\u003e\n\u003cli\u003eHempel, A. (1904). Notas sobre dois inimigos da laranjeira. Boletim da Agricultura, S\u0026atilde;o Paulo, 5, 10\u0026ndash;21. \u003c/li\u003e\n\u003cli\u003eHodges, G. S., \u0026amp; Evans, G. A. (2005). An identification guide to the whiteflies (Hemiptera: Aleyrodidae) of the southeastern United States. \u003cem\u003eFlorida Entomologist\u003c/em\u003e, 88(4), 518\u0026ndash;534. https://doi.org/10.1653/0015-4040(2005)88[518:AIGTTW]2.0.CO;2 \u003c/li\u003e\n\u003cli\u003eHuber, J. T. (2015). World reclassification of the \u003cem\u003eGonatocerus\u003c/em\u003e group of genera (Hymenoptera: Mymaridae). \u003cem\u003eZootaxa\u003c/em\u003e, 3967,(1), 1-184. \u003c/li\u003e\n\u003cli\u003eLouren\u0026ccedil;\u0026atilde;o, A. L., Costa, V. A., Pereira, L. S., \u0026amp; Prado, J. C. (2014). Occurrence of \u003cem\u003eEretmocerus mundus\u003c/em\u003e Mercet (Hymenoptera: Aphelinidae) parasitizing \u003cem\u003eBemisia tabaci\u003c/em\u003e (Genn.) biotype B (Hemiptera: Aleyrodidae) in Brazil. \u003cem\u003eBragantia\u003c/em\u003e, 73(2), 160\u0026ndash;162. https://doi.org/10.1 590/brag.2014.025\u003c/li\u003e\n\u003cli\u003eLouren\u0026ccedil;\u0026atilde;o, A. L., Fancelli, M., Costa, V. A., \u0026amp; Ribeiro, N. C. (2007). Parasitismo em \u003cem\u003eTrialeurodes variabilis\u003c/em\u003e (Quaintance) (Hemiptera: Aleyrodidae) por \u003cem\u003eEncarsia hispida\u003c/em\u003e De Santis (Hymenoptera: Aphelinidae), em mamoeiro, no Brasil. \u003cem\u003eNeotropical Entomology\u003c/em\u003e, 36(1), 147\u0026ndash;149. https://doi.org/10.1590/S1519-566X2007000100019\u003c/li\u003e\n\u003cli\u003eMartin, J. H., Mifsud, D., \u0026amp; Rapisarda, C. (2000). The whiteflies (Hemiptera: Aleyrodidae) of Europe and the Mediterranean Basin. \u003cem\u003eBulletin of Entomological Research\u003c/em\u003e, 90, (5), 407\u0026ndash;448. https://doi.org/10.1017/S0007485300000547 \u003c/li\u003e\n\u003cli\u003eMound, L. A., \u0026amp; Halsey, S. H. (1978). Whitefly of the world: a systematic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data. John Wiley \u0026amp; Sons, London. \u003c/li\u003e\n\u003cli\u003eMound, L. A., \u0026amp; Marullo, Y. R. (1996). The thrips of Central and South America: An Introduction (Insecta: Thysanoptera). \u003cem\u003eFlorida Entomologist\u003c/em\u003e, 79,(2), 1\u0026ndash;488. https://doi.org/10.2307/3495826 \u003c/li\u003e\n\u003cli\u003eMu\u0026ntilde;oz, R. G., \u0026amp; Be\u0026eacute;che, M. C. (1995). Antecedentes sobre dos esp\u0026eacute;cies de reciente identificacion para Chile (Homoptera: Aleyrodidae, Aphididae). \u003cem\u003eRevista Chilena de Entomolog\u0026iacute;a\u003c/em\u003e, 22, 89\u0026ndash;91. \u003c/li\u003e\n\u003cli\u003eNguyen, R., \u0026amp; Hamon, A.B. (2020). Ash whitefly. Available at: https://entnemdept.ufl.edu/creatures/orn/ash_whitefly.htm. Accessed 15 April 2023.\u003c/li\u003e\n\u003cli\u003eOliveira, M. R. V., Amancio, E., Laumann, R. A., \u0026amp; Gomes, L. O. (2003). Natural enemies of \u003cem\u003eBemisia tabaci\u003c/em\u003e (Gennadius) B biotype and \u003cem\u003eTrialeurodes vaporariorum\u003c/em\u003e (Westwood) (Hemiptera: Aleyrodidae) in Bras\u0026iacute;lia, Brazil. \u003cem\u003eNeotropical Entomology\u003c/em\u003e, 32(1), 151\u0026ndash;154. https://doi.org/10.1590/S1519-566X2003000100023\u003c/li\u003e\n\u003cli\u003eOliveira, R., Souza, M. S., Nunes, G. S., Batista, J. L., \u0026amp; Brito, C. H. (2019). Selectivity of insecticides to \u003cem\u003eEncarsia hispida\u003c/em\u003e (Hymenoptera: Aphelinidae). \u003cem\u003eRevista Caatinga\u003c/em\u003e, 32(2), 312\u0026ndash;317. http://dx.doi.org/10.1590/1983-21252019v32n203rc \u003c/li\u003e\n\u003cli\u003ePolaszek, A., Evans, G. A., \u0026amp; Bennett, F. D. (1992). \u003cem\u003eEncarsia\u003c/em\u003e parasitoids of \u003cem\u003eBemisia tabaci\u003c/em\u003e (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): a preliminary guide to identification. \u003cem\u003eBulletin of Entomological Research\u003c/em\u003e, 82(3), 375\u0026ndash;392. https://doi.org/10.1017/S0007485300041171\u003c/li\u003e\n\u003cli\u003ePolaszek, A., Manzari, S., \u0026amp; Quicke, D. L. J. (2004). Morphological and molecular taxonomic analysis of the \u003cem\u003eEncarsia meritoria\u003c/em\u003e species-complex (Hymenoptera, Aphelinidae), parasitoids of whiteflies (Hemiptera, Aleyrodidae) of economic importance. \u003cem\u003eZoologica Scripta\u003c/em\u003e, 33(5), 403\u0026ndash;421. https://doi.org/10.1111/j.0300-3256.2004.00161.x\u003c/li\u003e\n\u003cli\u003eSilvestri, F. (1915). Contributo alla conoscenza degli insetti dell olivo dell Eritrea e dell Africa meridionale. \u003cem\u003eBollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d\u0026apos;Agricultura\u003c/em\u003e, 9, 245\u0026ndash;249. \u003c/li\u003e\n\u003cli\u003eSimon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., \u0026amp; Flook, P. (1994). Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. \u003cem\u003eAnnals of the Entomological Society of America\u003c/em\u003e\u003cem\u003e, \u003c/em\u003e87(6), 651\u0026ndash;702. https://doi.org/10.1093/aesa/87.6.651\u003c/li\u003e\n\u003cli\u003eTorres, L. C., Louren\u0026ccedil;\u0026atilde;o, A. L., Costa, V. A., Souza, B., Costa, M. B., \u0026amp; Tanque, R. L. (2014). Records of natural enemies of \u003cem\u003eBemisia tabaci\u003c/em\u003e (Genn.) (Hemiptera: Aleyrodidae) Biotype B in Brazil. \u003cem\u003eNeotropical Entomology\u003c/em\u003e, 43(2), 189\u0026ndash;191. https://doi.org/10.1007/s13744-013-0188-3 \u003c/li\u003e\n\u003cli\u003eValencia, L. V. (2011). Reestablecimiento de \u003cem\u003eSiphoninus finitimus \u003c/em\u003eSilvestri (Hemiptera: Aleyrodidae) como una especie valida, en base a datos morfol\u0026oacute;gicos, plantas hospederas y parasitoides en el Per\u0026uacute;. \u003cem\u003eRevista Peruana de Entomolog\u0026iacute;a\u003c/em\u003e, 46(2), 59\u0026ndash;67. \u003c/li\u003e\n\u003cli\u003eViscarret, M.M., \u0026amp; Botto, E.N. (1997). Presencia de \u003cem\u003eSiphoninus phillyreae\u003c/em\u003e,\u0026quot;la mosca blanca de los fresnos\u0026quot; (Homoptera: Aleyrodidae) en la Argentina. \u003cem\u003eRevista de la Sociedad Entomologica Argentina\u003c/em\u003e 56, 1\u0026ndash;4. \u003c/li\u003e\n\u003cli\u003eWengrat, A. P. G. S, Coelho Junior, A., Parra, J. R. P., Takahashi, T. A., Foerster, L. A., Corr\u0026ecirc;a, A. S., Polaszek, A., Johnson, N. F., Costa, V. A., Zucchi, R. A. (2021). Integrative taxonomy and phylogeography of \u003cem\u003eTelenomus remus\u003c/em\u003e (Scelionidae), with the first record of natural parasitism of \u003cem\u003eSpodoptera\u003c/em\u003e spp. in Brazil. \u003cem\u003eScientific Reports\u003c/em\u003e, 11, 1\u0026ndash;9. https://doi.org/10.1038/s41598-021-93510-3\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Table 1","content":"\u003cp\u003e\u003cstrong\u003eTable 1.\u003c/strong\u003e Average temperature, rainfall, and sample size for ash whitefly, \u003cem\u003eSiphoninus phillyreae\u003c/em\u003e infesting pomegranate leaves in Brazil (2023-2024). \u0026nbsp; \u0026nbsp; \u0026nbsp;\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\" width=\"605\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd width=\"38.51239669421488%\"\u003e\n \u003cp\u003e\u003cstrong\u003eLocation\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"13.057851239669422%\"\u003e\n \u003cp\u003e\u003cstrong\u003eSamples\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"26.611570247933884%\"\u003e\n \u003cp\u003e\u003cstrong\u003eAverage temperature\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"21.818181818181817%\"\u003e\n \u003cp\u003e\u003cstrong\u003eAverage rainfall\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"38.51239669421488%\"\u003e\n \u003cp\u003e\u003cstrong\u003ePiracicaba - SP\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"13.057851239669422%\" valign=\"top\"\u003e\n \u003cp\u003e4.00\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"26.611570247933884%\" valign=\"top\"\u003e\n \u003cp\u003e23.60\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"21.818181818181817%\" valign=\"top\"\u003e\n \u003cp\u003e0.03\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"38.51239669421488%\"\u003e\n \u003cp\u003e\u003cstrong\u003ePlanaltina - GO\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"13.057851239669422%\" valign=\"top\"\u003e\n \u003cp\u003e1.00\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"26.611570247933884%\" valign=\"top\"\u003e\n \u003cp\u003e21.30\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"21.818181818181817%\" valign=\"top\"\u003e\n \u003cp\u003e0.34\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"38.51239669421488%\"\u003e\n \u003cp\u003e\u003cstrong\u003eFloriano - PI\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"13.057851239669422%\" valign=\"top\"\u003e\n \u003cp\u003e1.00\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"26.611570247933884%\" valign=\"top\"\u003e\n \u003cp\u003e26.90\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"21.818181818181817%\" valign=\"top\"\u003e\n \u003cp\u003e0.9\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"38.51239669421488%\"\u003e\n \u003cp\u003e\u003cstrong\u003eS\u0026atilde;o Jo\u0026atilde;o dos Patos - MA\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"13.057851239669422%\" valign=\"top\"\u003e\n \u003cp\u003e1.00\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"26.611570247933884%\" valign=\"top\"\u003e\n \u003cp\u003e28.50\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"21.818181818181817%\" valign=\"top\"\u003e\n \u003cp\u003e0.00\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"38.51239669421488%\"\u003e\n \u003cp\u003e\u003cstrong\u003eJana\u0026uacute;ba - MG\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"13.057851239669422%\" valign=\"top\"\u003e\n \u003cp\u003e1.00\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"26.611570247933884%\" valign=\"top\"\u003e\n \u003cp\u003e24.40\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"21.818181818181817%\" valign=\"top\"\u003e\n \u003cp\u003e0.53\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"phytoparasitica","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"pypa","sideBox":"Learn more about [Phytoparasitica](http://link.springer.com/journal/12597)","snPcode":"12600","submissionUrl":"https://submission.nature.com/new-submission/12600/3","title":"Phytoparasitica","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Crops, Invasive species, Pomegranate, Punica granatum","lastPublishedDoi":"10.21203/rs.3.rs-4849950/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4849950/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e \u003cem\u003eSiphoninus phillyreae\u003c/em\u003e (Haliday) (Hemiptera: Aleyrodidae) is a polyphagous species with a wide geographical distribution and high invasion potential. In South America, it has been documented in Venezuela, Chile, Peru and Argentina. Pomegranate leaves [\u003cem\u003ePunica granatum\u003c/em\u003e L. (Lythraceae)] containing whitefly eggs, nymphs, puparia, and adults were collected in the municipalities of Campinas, Piracicaba (S\u0026atilde;o Paulo), Planaltina (Goi\u0026aacute;s), S\u0026atilde;o Jo\u0026atilde;o dos Patos (Maranh\u0026atilde;o), Floriano (Piau\u0026iacute;), and Jana\u0026uacute;ba (Minas Gerais). Based on morphological characters, the species was identified as \u003cem\u003eS. phillyreae\u003c/em\u003e in the collections. Additionally, parasitism by \u003cem\u003eEncarsia brasiliensis\u003c/em\u003e (Hempel) was observed in Piracicaba. The adults collected in Piracicaba underwent molecular characterization, validating the morphological identification. In Brazil, the pomegranate tree is often grown as an ornamental plant in gardens due to the beauty of its leaves, flowers, fruits, and medicinal properties. Thus, due to the increase in pomegranate cultivation, an appropriate management plan for this pest is necessary. Therefore, this is the first record of the \u003cem\u003eS. phillyreae\u003c/em\u003e in Brazil, expanding its distribution in South America.\u003c/p\u003e","manuscriptTitle":"Submission to: Phytoparasitica Occurrence of ash whitefly, Siphoninus phillyreae (Haliday) (Hemiptera: Aleyrodidae), in Brazil","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-09-02 10:48:49","doi":"10.21203/rs.3.rs-4849950/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Accepted","date":"2025-02-17T13:21:13+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-02-15T19:10:57+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"95446356266613791620223198418223086124","date":"2025-02-11T02:34:51+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"50885810638238683566979724019291172241","date":"2025-02-10T16:40:13+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-01-02T01:22:25+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"47516768359281063913413121948200589289","date":"2024-12-10T04:48:11+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"13467781627325181405224078488675719637","date":"2024-11-08T00:01:19+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-09-02T02:34:30+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"194609994606105568623994299958934577986","date":"2024-08-12T14:27:37+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-08-09T15:02:22+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-08-07T00:02:21+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-08-06T01:07:42+00:00","index":"","fulltext":""},{"type":"submitted","content":"Phytoparasitica","date":"2024-08-02T17:33:57+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"phytoparasitica","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"pypa","sideBox":"Learn more about [Phytoparasitica](http://link.springer.com/journal/12597)","snPcode":"12600","submissionUrl":"https://submission.nature.com/new-submission/12600/3","title":"Phytoparasitica","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"bf529286-e7d6-4b62-955e-0b6a639962ce","owner":[],"postedDate":"September 2nd, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2025-03-24T16:09:16+00:00","versionOfRecord":{"articleIdentity":"rs-4849950","link":"https://doi.org/10.1007/s12600-025-01255-w","journal":{"identity":"phytoparasitica","isVorOnly":false,"title":"Phytoparasitica"},"publishedOn":"2025-03-20 15:58:06","publishedOnDateReadable":"March 20th, 2025"},"versionCreatedAt":"2024-09-02 10:48:49","video":"","vorDoi":"10.1007/s12600-025-01255-w","vorDoiUrl":"https://doi.org/10.1007/s12600-025-01255-w","workflowStages":[]},"version":"v1","identity":"rs-4849950","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4849950","identity":"rs-4849950","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}