{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,8]],"date-time":"2026-04-08T05:38:18Z","timestamp":1775626698763,"version":"3.50.1"},"reference-count":50,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T00:00:00Z","timestamp":1733961600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["140905\/2020\u20130"],"award-info":[{"award-number":["140905\/2020\u20130"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["306486\/2019\u20139"],"award-info":[{"award-number":["306486\/2019\u20139"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","doi-asserted-by":"publisher","award":["88887.903938\/2023-00"],"award-info":[{"award-number":["88887.903938\/2023-00"]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Edessinae is one of the ten subfamilies of Pentatomidae, and it is further divided into seven genera. Among these, <jats:italic>Edessa<\/jats:italic> Fabricius, 1803 is the most diverse genus, boasting around 300 species recognized for their ecological and economic significance worldwide. The inclusion of various pentatomids in the <jats:italic>Edessa<\/jats:italic> genus has led to mistakes in its taxonomy due to common morphological features and misidentifications. An alternative to avoid mistakes is to use diverse datasets to characterize and classify insects, such as the male reproductive system and sperm morphology, for their variability and conserved traits within a clade. Thus, we described the morphology of the male reproductive system, spermatozoa, and spermiogenesis of <jats:italic>Edessa rufomarginata<\/jats:italic> (De Geer, 1773) using light microscopy. We discovered that their male reproductive system consists of a pair of elongated testes with four follicles each. The analysis revealed for the first time the presence of dimorphic spermatozoa in Edessinae. There are two distinct morphotypes: spermatozoa type I, produced by follicles 1, 2, and 3, with a total length of approximately 325 \u03bcm and a nucleus of 34 \u03bcm and spermatozoa type II, produced by follicle 4, measuring approximately 156 \u03bcm in total length and 73 \u03bcm in the nucleus, and showing an aberrant sperm morphology with different morphology from what has been described in Pentatomidae. The presence of sperm dimorphism in <jats:italic>E<\/jats:italic>. <jats:italic>rufomarginata<\/jats:italic> are not reported in any other Pentatomidae to date, and it may contribute to establishing taxonomic limits within the subfamily Edessinae.<\/jats:p>","DOI":"10.1371\/journal.pone.0311254","type":"journal-article","created":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T18:45:28Z","timestamp":1734029128000},"page":"e0311254","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["First report of aberrant sperm in Edessinae and analysis of the male reproductive system of Edessa rufomarginata (De Geer, 1773) (Hemiptera: Pentatomidae)"],"prefix":"10.1371","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3017-3987","authenticated-orcid":true,"given":"Mauricio da Silva","family":"Paulo","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2919-0218","authenticated-orcid":true,"given":"Paulo Henrique","family":"Rezende","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1641-2870","authenticated-orcid":true,"given":"Dayvson Ayala","family":"Costa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1417-0011","authenticated-orcid":true,"given":"Ana Clara Pereira","family":"Teixeira","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6027-2118","authenticated-orcid":true,"given":"Francisco Witallo Sousa do","family":"Nascimento","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jos\u00e9","family":"Lino-Neto","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1455-6398","authenticated-orcid":true,"given":"Glenda","family":"Dias","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2024,12,12]]},"reference":[{"key":"pone.0311254.ref001","volume-title":"Classification and Natural History","author":"RT Schuh","year":"1995"},{"issue":"6","key":"pone.0311254.ref002","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1111\/j.1096-0031.2008.00224.x","article-title":"Phylogenetic relationships of family groups in Pentatomoidea based on morphology and DNA sequences (Insecta: Heteroptera)","volume":"24","author":"J Grazia","year":"2008","journal-title":"Cladistics"},{"issue":"3","key":"pone.0311254.ref003","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1590\/S0073-47212006000300012","article-title":"Caracteriza\u00e7\u00e3o do grupo Edessa rufomarginata e descri\u00e7\u00e3o de sete novas esp\u00e9cies (Heteroptera, Pentatomidae, Edessinae)","volume":"96","author":"EJE Silva","year":"2006","journal-title":"Iheringia\u2014S\u00e9rie Zoologia"},{"key":"pone.0311254.ref004","volume-title":"Entomology in Focus","author":"AR Panizzi","year":"2015"},{"issue":"1","key":"pone.0311254.ref005","first-page":"628","article-title":"A new species group to Edessa, the E. ovina group, with description of a new species (Heteroptera: Pentatomidae: Edessinae) from Brazil","volume":"4958","author":"JAM Fernandes","year":"2021","journal-title":"Zootaxa"},{"issue":"5","key":"pone.0311254.ref006","first-page":"441","article-title":"Proposition of a new species group in Edessa Fabricius, 1803 (Hemiptera: Heteroptera: Pentatomidae: Edessinae)","volume":"3774","author":"BTS Santos","year":"2014","journal-title":"Zootaxa"},{"issue":"8","key":"pone.0311254.ref007","first-page":"151","article-title":"The E. cervus-group of Edessa Fabricius, 1803 (Heteroptera: Pentatomidae: Edessinae)","volume":"74","author":"JAM Fernandes","year":"2000","journal-title":"Zoologische Mededeligen"},{"issue":"1","key":"pone.0311254.ref008","first-page":"139","article-title":"The Male Reproductive Organs of Nezara viridula (L.) with a Preliminar Account of Their Development (Heteroptera; Pentatomidae). Auckland University College","volume":"84","author":"JG Pendergrast","year":"1956","journal-title":"Transactions of the Royal Society of New Zealand"},{"issue":"3","key":"pone.0311254.ref009","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1590\/S1676-06032013000300016","article-title":"Morphological aspects of the testes of 18 species of terrestrial of Heteroptera from Northwestern S\u00e3o Paulo (Brazil)","volume":"13","author":"MO Gomes","year":"2013","journal-title":"Biota Neotropica"},{"issue":"3","key":"pone.0311254.ref010","doi-asserted-by":"crossref","first-page":"500","DOI":"10.11646\/zootaxa.3937.3.4","article-title":"Morphology of spermathecae of some pentatomids (Hemiptera: Heteroptera: Pentatomidae) from Turkey","volume":"3937","author":"S Candan","year":"2015","journal-title":"Zootaxa"},{"issue":"6","key":"pone.0311254.ref011","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1016\/j.micron.2011.02.001","article-title":"Ultrastructure and heteromorphism of spermatozoa in five species of bugs (Pentatomidae: Heteroptera)","volume":"42","author":"VA Ara\u00fajo","year":"2011","journal-title":"Elsevier. Micron"},{"issue":"12","key":"pone.0311254.ref012","doi-asserted-by":"crossref","first-page":"42","DOI":"10.15373\/22778179\/DEC2013\/14","article-title":"The Morphology and Histology of The Female Reproductive System of Graphosoma lineatum (Heteroptera: Pentatomidae) based on light and scanning electron microscope studies","volume":"2","author":"N \u00d6zyurt","year":"2013","journal-title":"IJSR\u2014International Journal of Scientific Research"},{"issue":"1","key":"pone.0311254.ref013","first-page":"31","article-title":"The morphology and histology of the male reproductive system in Apodiphus amygdali (Germar, 1817) (Hemiptera: Heteroptera: Pentatomidae)","volume":"2","author":"N \u00d6zyurt","year":"2014","journal-title":"Life: The Excitement of Biology"},{"issue":"8","key":"pone.0311254.ref014","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1002\/jemt.22514","article-title":"Ultrastructure of Male Reproductive System of Eurydema ventrale Kolenati 1846 (Heteroptera: Pentatomidae)","volume":"78","author":"N \u00d6zyurt","journal-title":"Microscopy Research and Technique"},{"issue":"4","key":"pone.0311254.ref015","doi-asserted-by":"crossref","first-page":"e20201045","DOI":"10.1590\/1676-0611-bn-2020-1045","article-title":"Anatomy of male and female reproductive organs of stink bugs pests (Pentatomidae: Heteroptera) from soybean and rice crops","volume":"20","author":"VA Ara\u00fajo","year":"2020","journal-title":"Biota Neotropica"},{"key":"pone.0311254.ref016","doi-asserted-by":"crossref","first-page":"71","DOI":"10.3897\/zookeys.1136.96431","article-title":"A synopsis of the numbers of testicular follicles and ovarioles in true bugs (Heteroptera, Hemiptera)\u2013Sixty-five years of progress after J","volume":"1136","author":"S Grozeva","year":"2022","journal-title":"Pendergrast\u2019s Review. ZooKeys"},{"key":"pone.0311254.ref017","volume-title":"Insects: their spermatozoa and phylogeny","author":"BGM Jamieson","year":"1999"},{"key":"pone.0311254.ref018","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev-ento-010715-023555","article-title":"Structure and evolution of insect sperm: new interpretations in the age of phylogenomics","volume":"61","author":"R Dallai","year":"2016","journal-title":"Annual Review of Entomology"},{"issue":"4","key":"pone.0311254.ref019","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1111\/jzs.12136","article-title":"The evolution of insect sperm\u2014an unusual character system in a megadiverse group","volume":"54","author":"M Gottardo","year":"2016","journal-title":"Journal of Zoological Systematics and Evolutionary Research"},{"issue":"16","key":"pone.0311254.ref020","doi-asserted-by":"crossref","first-page":"391","DOI":"10.2307\/20025937","article-title":"Studies on Insect Spermatogenesis. IV. 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Schrader","year":"1960a","journal-title":"Chromosoma"},{"issue":"4","key":"pone.0311254.ref023","doi-asserted-by":"crossref","first-page":"498","DOI":"10.2307\/2405998","article-title":"Evolutionary aspects of aberrant meiosis in some Pentatominae (Heteroptera)","volume":"14","author":"F. Schrader","year":"1960","journal-title":"Evolution\u2014International Journal of Organic Evolution"},{"issue":"2","key":"pone.0311254.ref024","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1017\/S1464793101005851","article-title":"The long and short of sperm polymorphisms in insects","volume":"77","author":"JG Swallow","year":"2002","journal-title":"Biological Reviews"},{"issue":"84","key":"pone.0311254.ref025","first-page":"1","article-title":"Sperm sizer: A program to semi-automate the measurement of sperm length","volume":"75","author":"CS McDiarmid","year":"2021","journal-title":"Behavioral Ecology Sociobiology"},{"issue":"3","key":"pone.0311254.ref026","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/0014-4827(50)90020-6","article-title":"A cytochemical analysis of the functional interrelations of various cell structures in Arvelius albopuntatus (De Geer)","volume":"1","author":"F Schrader","year":"1950","journal-title":"Experimental Cell Research"},{"key":"pone.0311254.ref027","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1007\/BF00325782","article-title":"The cytology and chemical nature of some constituents of the developing sperm","volume":"4","author":"F Schrader","year":"1951","journal-title":"Chromosoma"},{"issue":"1","key":"pone.0311254.ref028","first-page":"1","article-title":"Comparative Study of Spermatogenesis and Nucleolar Behavior in Testicular Lobes of Euschistus heros (Heteroptera: Pentatomidae)","volume":"2010","author":"HV Souza","year":"2010","journal-title":"Psyche: A Journal of Entomology"},{"issue":"3","key":"pone.0311254.ref029","doi-asserted-by":"crossref","first-page":"10","DOI":"10.5539\/jas.v15n3p10","article-title":"Morphological and Morphometric Parameters of the Reproductive Organs of Euschistus heros (Hemiptera: Pentatomidae) Treated with a Sublethal Juvenile Hormone Analog","volume":"15","author":"PSG Cremonez","year":"2023","journal-title":"Journal of Agricultural Science"},{"issue":"3","key":"pone.0311254.ref030","first-page":"445","article-title":"Revision of Ascra with proposition of the bifida species group and description of two new species (Hemiptera: Pentatomidae: Edessinae)","volume":"4034","author":"BTS Santos","year":"2015","journal-title":"Zootaxa"},{"key":"pone.0311254.ref031","doi-asserted-by":"crossref","first-page":"63","DOI":"10.2307\/1538172","article-title":"Regular occurrence of heteroploidy in a group of Pentatomidae (Hemiptera)","volume":"88","author":"F. Schrader","year":"1945","journal-title":"Biological Bulletin"},{"key":"pone.0311254.ref032","first-page":"69","volume-title":"Sperm Biology: an evolutionary perspective","author":"S Pitnick"},{"key":"pone.0311254.ref033","doi-asserted-by":"crossref","DOI":"10.4159\/harvard.9780674330702","volume-title":"Sexual Selection and Animal Genitalia","author":"WG Eberhard","year":"1985"},{"issue":"1523","key":"pone.0311254.ref034","doi-asserted-by":"crossref","first-page":"1507","DOI":"10.1098\/rspb.2003.2382","article-title":"Ejaculate-female coevolution in Drosophila mojavensis","volume":"270","author":"S Pitnick","year":"2003","journal-title":"Proceedings. Biological Sciences"},{"issue":"1813","key":"pone.0311254.ref035","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1098\/rstb.2020.0061","article-title":"Conceptual developments in sperm competition: a very brief synopsis","volume":"375","author":"GA Parker","year":"2020","journal-title":"Philosophical Transactions of the Royal Society B"},{"issue":"4","key":"pone.0311254.ref036","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/0022-1910(95)00109-3","article-title":"Drosophila subobscura females preferentially select long sperm for storage and use","volume":"42","author":"C Bressac","year":"1996","journal-title":"Journal of Insect Physiology"},{"key":"pone.0311254.ref037","first-page":"165","article-title":"Ultrastructural and cytochemical analysis of sperm dimorphism in Drosophila subobscura. Tissue &","volume":"28","author":"ME Pasini","year":"1996","journal-title":"Cell"},{"issue":"2","key":"pone.0311254.ref038","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1603\/008.102.0212","article-title":"Stages of gonadal development of the southern green stink bug (Hemiptera: Pentatomidae): improved visualization","volume":"102","author":"JF Esquivel","year":"2009","journal-title":"Annals of the Entomological Society of America"},{"issue":"3","key":"pone.0311254.ref039","doi-asserted-by":"crossref","first-page":"176","DOI":"10.9734\/ARRB\/2015\/14941","article-title":"Revamp studies on morpho-histology of the male reproductive system of Halys dentatus Fabricius (Hemiptera: Pentatomidae)","volume":"63","author":"G Jyoti","year":"2015","journal-title":"Annual Research & Review in Biology"},{"issue":"3","key":"pone.0311254.ref040","doi-asserted-by":"crossref","first-page":"333","DOI":"10.14411\/eje.2011.041","article-title":"Comparative analysis of the testes and spermatogenesis in species of the family Pentatomidae (Heteroptera)","volume":"108","author":"HV Souza","year":"2011","journal-title":"European Journal of Entomology"},{"key":"pone.0311254.ref041","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1007\/s00435-021-00525-5","article-title":"Male reproductive system and sperm morphology of Eccritotarsini plant bugs (Heteroptera: Miridae)","volume":"140","author":"PH Rezende","year":"2021","journal-title":"Zoomorphology"},{"key":"pone.0311254.ref042","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1007\/978-1-4613-2715-8_10","volume-title":"Insect Ultrastructure","author":"GM Happ","year":"1984"},{"issue":"3","key":"pone.0311254.ref043","first-page":"255","article-title":"Microtubules as components of Drosophila male paragonia secretion: An electron microscopic study, with enzymatic tests","volume":"3","author":"ME Perotti","year":"1971","journal-title":"Journal of Submicroscopic Cytology"},{"issue":"1","key":"pone.0311254.ref044","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/0022-1910(73)90234-5","article-title":"Ultrastructure of the ejaculatory duct region producing the male housefly accessory material","volume":"19","author":"JG Reimann","year":"1973","journal-title":"Journal of Insect Physiology"},{"issue":"2","key":"pone.0311254.ref045","first-page":"225","article-title":"Fertilization in the honey-bee. 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The male sexual organs: Their histological structure and physiological functioning","volume":"31","author":"GH Bishop","year":"1920","journal-title":"Journal of Experimental Zoology"},{"key":"pone.0311254.ref046","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/B978-012100543-6\/50035-0","volume-title":"Sexual Selection and Sperm Competition","author":"L Simmons","year":"1998"},{"key":"pone.0311254.ref047","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1146\/annurev.en.21.010176.001215","article-title":"The role of male accessory glands in insect reproduction","volume":"21","author":"RA Leopold","year":"1976","journal-title":"Annual Review of Entomology"},{"issue":"2","key":"pone.0311254.ref048","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1179\/2047773212Y.0000000016","article-title":"Function and composition of male accessory gland secretions in Anopheles gambiae: a comparison with other insect vectors of infectious diseases","volume":"106","author":"F Baldini","year":"2012","journal-title":"Pathogens and Global Health"},{"issue":"3","key":"pone.0311254.ref049","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1002\/jemt.23406","article-title":"Accessory glands of male reproductive system in Pseudochorthippus parallelus parallelus (Zetterstedt, 1821) (Orthoptera: Acrididae): A light and electron microscopic study","volume":"83","author":"I Polat","year":"2019","journal-title":"Microscopy Research and Technique"},{"issue":"2","key":"pone.0311254.ref050","doi-asserted-by":"crossref","first-page":"132","DOI":"10.3390\/insects14020132","article-title":"Proteome Analysis of Male Accessory Gland Secretions in the Diamondback Moth, Plutella xylostella (Lepidoptera: Plutellidae)","volume":"14","author":"LJ Wu","year":"2023","journal-title":"Insects"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0311254","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T18:46:19Z","timestamp":1734029179000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0311254"}},"subtitle":[],"editor":[{"given":"Abeer","family":"El Wakil","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2024,12,12]]},"references-count":50,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2024,12,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0311254","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,12]]}}}