{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T21:34:27Z","timestamp":1785879267096,"version":"3.56.0"},"reference-count":47,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2022,6,23]],"date-time":"2022-06-23T00:00:00Z","timestamp":1655942400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100016706","name":"Pennsylvania Soybean Board","doi-asserted-by":"publisher","award":["PSB # R2017-P05"],"award-info":[{"award-number":["PSB # R2017-P05"]}],"id":[{"id":"10.13039\/100016706","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Soybean thrips (Neohydatothrips variabilis) are an important phytophagous vector of the widely recognized Soybean vein necrosis orthotospovirus (SVNV). Understanding the egg-laying behavior of these thrips could aid in developing strategies for the management of the vector and virus. In this study, we described the egg-laying behavior of N. variabilis and reconstructed the three-dimensional morphology of the female terminalia by using serial block-face scanning electron microscopy (SBFSEM) and confocal laser scanning microscopy (CLSM). The female reproductive system consists of two panoistic ovaries consisting of eight ovarioles. The appendage gland is connected to the ovaries by two muscles, and to the body wall by a single muscle. The spermatheca is connected to the eighth tergum through four branched muscles, to the basivalvulae of the ovipositor by one muscle and to the vagina by a single muscle. The external genitalia are operated by seven muscles. The movement of the eggs inside the ovipositor is achieved by the back and forth \u201crocking\u201d movement of the first valvulae and valvifer. Eggs are deposited into the parenchymatous tissue alongside leaf veins. To the best of our knowledge, this is the first study describing the internal and external genitalia of N. variabilis.<\/jats:p>","DOI":"10.3390\/insects13070566","type":"journal-article","created":{"date-parts":[[2022,6,23]],"date-time":"2022-06-23T21:25:00Z","timestamp":1656019500000},"page":"566","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Morphology of the Female Reproductive System of the Soybean Thrips, Neohydatothrips variabilis (Beach, 1896) (Thysanoptera: Thripidae)"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6900-0661","authenticated-orcid":false,"given":"Asifa","family":"Hameed","sequence":"first","affiliation":[{"name":"Entomology, The Pennsylvania State University, 501 ASI, University Park, State College, PA 16802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonah M.","family":"Ulmer","sequence":"additional","affiliation":[{"name":"Entomology, State Museum of Natural History Stuttgart, Rosenstein 1, 70191 Stuttgart, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Istvan","family":"Miko","sequence":"additional","affiliation":[{"name":"Biological Sciences, University of New Hampshire Durham, Spaulding Hall Rm 266, Durham, NH 03824, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4990-1507","authenticated-orcid":false,"given":"Cristina","family":"Rosa","sequence":"additional","affiliation":[{"name":"Plant Pathology and Environmental Microbiology, Pennsylvania State University, University Park, State College, PA 16802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edwin G.","family":"Rajotte","sequence":"additional","affiliation":[{"name":"Entomology, The Pennsylvania State University, 501 ASI, University Park, State College, PA 16802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/bs.aiip.2018.07.005","article-title":"Screening, efficacy and mechanisms of microbial control agents against sucking pest insects as thrips","volume":"55","author":"Wu","year":"2018","journal-title":"Adv. Insect Physiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"77","DOI":"10.57182\/jbiopestic.7.1.77-84","article-title":"Impact of entomopathogenic nematodes on Thrips tabaci Lindeman (Thysanoptera: Thripidae) life stages in the laboratory and under semi-field conditions","volume":"7","author":"Kashkouli","year":"2014","journal-title":"J. Biopestic."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"867","DOI":"10.1016\/S1671-2927(11)60073-4","article-title":"Thrips: Pests of concern to China and the United States","volume":"10","author":"Stuart","year":"2011","journal-title":"Agric. Sci. China"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"395","DOI":"10.11646\/zootaxa.1668.1.21","article-title":"The insect order Thysanoptera: Classification versus systematics","volume":"1668","author":"Mound","year":"2007","journal-title":"Zootaxa"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1007\/s11262-011-0621-9","article-title":"Molecular characterization of a new tospovirus infecting soybean","volume":"43","author":"Zhou","year":"2011","journal-title":"Virus Genes"},{"key":"ref_6","first-page":"133","article-title":"Seasonal population dynamics of Thrips (Thysanoptera) in Wisconsin and Iowa soybean fields","volume":"110","author":"Bloomingdale","year":"2016","journal-title":"J. Econ. Entomol."},{"key":"ref_7","unstructured":"Irizarry, M. (2016). Soybean Vein Necrosis Virus: Impacts of Infection on Yield Loss and Seed Quality and Expansion of Plant Host Range. [Ph.D. Thesis, Iowa State University]."},{"key":"ref_8","unstructured":"Keough, S.A. (2015). Surveying Indiana Soybean for Soybean vein necrosis virus (SVNV) and Analysis of SVNV on Life History Traits and Host Preference of Thrips Vectors. [Ph.D. Thesis, Purdue University]."},{"key":"ref_9","unstructured":"Bloomingdale, C., Bradley, C., Chilvers, M., Giesler, L., Groves, R., Mueller, D., Smith, D., Tenuta, A., and Wise, K. (2015). An Overview of Soybean Vein Necrosis Virus, Crop Protection Network."},{"key":"ref_10","first-page":"76","article-title":"Identification and characterization of soybean vein necrosis virus (SVNV): A newly isolated thrips-borne tospovirus in Egypt","volume":"1","year":"2017","journal-title":"J. Virol. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Abd El-Wahab, A. (2021). Molecular characterization and incidence of new tospovirus: Soybean Vein Necrosis Virus (SVNV) in Egypt. Braz. J. Biol., 84.","DOI":"10.1590\/1519-6984.246460"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1094\/PHYTO-12-12-0322-R","article-title":"Epidemiology of Soybean vein necrosis-associated virus","volume":"103","author":"Zhou","year":"2013","journal-title":"Phytopathology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1007\/s11262-018-1618-4","article-title":"Soybean vein necrosis virus: An emerging virus in North America","volume":"55","author":"Zhou","year":"2019","journal-title":"Virus Genes"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1080\/07060661.2017.1354333","article-title":"Effect of soybean vein necrosis on yield and seed quality of soybean","volume":"39","author":"Anderson","year":"2017","journal-title":"Can. J. Plant Pathol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1093\/jee\/69.4.514","article-title":"Estimation of yield losses in cassava following attack from thrips","volume":"69","author":"Schoonhoven","year":"1976","journal-title":"J. Econ. Entomol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1007\/s002650050495","article-title":"High relatedness and inbreeding in two species of haplodiploid eusocial thrips (Insecta: Thysanoptera) revealed by microsatellite analysis","volume":"43","author":"Chapman","year":"1998","journal-title":"Behav. Ecol. Sociobiol."},{"key":"ref_17","first-page":"83","article-title":"Frankliniella occidentalis (Thysanoptera: Thripidae)\u2014A new pest in Danish glasshouses","volume":"93","year":"1989","journal-title":"Tidsskr. Planteavl."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1264","DOI":"10.1093\/ee\/35.5.1264","article-title":"Reproductive modes in onion thrips (Thysanoptera: Thripidae) populations from New York onion fields","volume":"35","author":"Nault","year":"2006","journal-title":"Environ. Entomol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Leskey, T.C., Teulon, D.A., and Cameron, E.A. (1995). Position and Abundance of Pear Thrips Eggs in Sugar Maple Flowering and Vegetative Buds. Thrips Biology and Management, Springer.","DOI":"10.1007\/978-1-4899-1409-5_11"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Heming, B.S. (1995). History of the Germ Line in Male and Female Thrips. Thrips Biology and Management, Springer.","DOI":"10.1007\/978-1-4899-1409-5_79"},{"key":"ref_21","unstructured":"Bailey, S.F., and Bailey, S.F. (1957). The Thrips of California, University of California Press."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Stannard, L.J. (1968). The thrips, or Thysanoptera, of Illinois. Illinois Natural History Survey Bulletin, Illinois Natural History Survey. No. 04.","DOI":"10.21900\/j.inhs.v29.166"},{"key":"ref_23","first-page":"3769","article-title":"Thrips (Thysanoptera)","volume":"Volume 4","author":"Tipping","year":"2008","journal-title":"Encyclopedia of Entomology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/s10340-012-0423-4","article-title":"Traditional and modern methods for the identification of thrips (Thysanoptera) species","volume":"85","author":"Mehle","year":"2012","journal-title":"J. Pest Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"12775","DOI":"10.1073\/pnas.1815820115","article-title":"Phylogenomics and the evolution of hemipteroid insects","volume":"115","author":"Johnson","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Parrella, M.P. (1995). IPM\u2014Approaches and prospects. Thrips Biology and Management, Springer.","DOI":"10.1007\/978-1-4899-1409-5_55"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1111\/j.1365-2311.1954.tb00763.x","article-title":"The external morphology of Chirothrips hamatus (Tryborn) (Thysanoptera)","volume":"105","author":"Jones","year":"1954","journal-title":"Trans. R. Ent Society London"},{"key":"ref_28","first-page":"541","article-title":"Anatomie und Biologie der Physapoda","volume":"47","author":"Jordan","year":"1888","journal-title":"Z. Wiss. Zool"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF00290072","article-title":"Der Ovipositor und die weiblichen geschlechtswege der Thripiden (Thysanoptera, Terebrantia)","volume":"81","author":"Bode","year":"1975","journal-title":"Z. Morphol. Tiere"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1111\/j.1365-3113.2012.00650.x","article-title":"Phylogeny of thrips (Insecta: Thysanoptera) based on five molecular loci","volume":"38","author":"Buckman","year":"2013","journal-title":"Syst. Entomol."},{"key":"ref_31","unstructured":"Hoddle, M.S., Mound, M.L., and Paris, D.L. (2012). Thrips of California\u2014Lucid Key Server, CBIT Publishing. Available online: https:\/\/keys.lucidcentral.org\/keys\/v3\/thrips_of_california\/Thrips_of_California.html."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1819","DOI":"10.1093\/jee\/81.6.1819","article-title":"Technique for staining leafhopper (Homoptera: Cicadellidae) salivary sheaths and eggs within unsectioned plant tissue","volume":"81","author":"Backus","year":"1988","journal-title":"J. Econ. Entomol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1002\/j.1537-2197.1936.tb09048.x","article-title":"A method of demonstrating rust hyphae and haustoria in unsectioned leaf tissue","volume":"23","author":"McBryde","year":"1936","journal-title":"Am. J. Bot."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1111\/j.1365-2311.1969.tb00519.x","article-title":"The skeletal musculature and its metamorphosis in Limothrips cerealium Haliday (Thysanoptera: Thripidae)","volume":"121","author":"Davies","year":"1969","journal-title":"Trans. R. Entomol. Soc. Lond."},{"key":"ref_35","unstructured":"Snodgrass, R. (1935). Principles of Insect Morphology, McGraw-Hill Book Company."},{"key":"ref_36","unstructured":"Snodgrass, R.E. (2018). Principles of Insect Morphology, Cornell University Press."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"100914","DOI":"10.1016\/j.asd.2020.100914","article-title":"From lanceolate to plate-like: Gross morphology, terminology, and evolutionary trends of the trichophoran ovipositor","volume":"54","author":"Zhou","year":"2020","journal-title":"Arthropod Struct. Dev."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1002\/mrd.22489","article-title":"The ImageJ ecosystem: An open platform for biomedical image analysis","volume":"82","author":"Schindelin","year":"2015","journal-title":"Mol. Reprod. Dev."},{"key":"ref_40","first-page":"6","article-title":"NCMIR methods for 3D EM: A new protocol for preparation of biological specimens for serial block face scanning electron microscopy","volume":"1","author":"Deerinck","year":"2010","journal-title":"Microscopy"},{"key":"ref_41","first-page":"1","article-title":"Structure and functional morphology of the ovipositor of Homolobus truncator (Hymenoptera: Ichneumonoidea: Braconidae)","volume":"18","author":"Boring","year":"2009","journal-title":"J. Hymenopt. Res."},{"key":"ref_42","first-page":"1","article-title":"Tisantteri italiani Genus Melanthrips","volume":"20","author":"Melis","year":"1993","journal-title":"Redia"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1111\/j.1365-2311.1961.tb00800.x","article-title":"The comparative morphology of the insect ovipositor","volume":"113","author":"Scudder","year":"1961","journal-title":"Trans. R. Entomol. Soc. Lond."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1111\/j.1365-2311.1959.tb02873.x","article-title":"The female genitalia of the heteroptera: Morphology and bearing on classification 1","volume":"111","author":"Scudder","year":"1959","journal-title":"Trans. R. Entomol. Soc. Lond."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"25","DOI":"10.3897\/jhr.33.5204","article-title":"Morphology and function of the ovipositor mechanism in Ceraphronoidea (Hymenoptera, Apocrita)","volume":"33","author":"Ernst","year":"2013","journal-title":"J. Hymenopt. Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1080\/13887890.2011.568190","article-title":"Ovipositor morphology and egg laying behaviour in the dragonfly Lestes macrostigma (Zygoptera: Lestidae)","volume":"14","author":"Matushkina","year":"2011","journal-title":"Int. J. Odonatol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1080\/00222939200770611","article-title":"New diagnostic ovipositor characters for doryctine wasps (Hymenoptera, Braconidae)","volume":"26","author":"Quicke","year":"1992","journal-title":"J. Nat. Hist."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/13\/7\/566\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:38:28Z","timestamp":1760139508000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/13\/7\/566"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,23]]},"references-count":47,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["insects13070566"],"URL":"https:\/\/doi.org\/10.3390\/insects13070566","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,23]]}}}