{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T11:30:47Z","timestamp":1787311847408,"version":"build-2736575974"},"reference-count":52,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,4,26]],"date-time":"2023-04-26T00:00:00Z","timestamp":1682467200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Senotainia tricuspis (Meigen, 1838) is a Sarcophagid dipteran endoparasitoid of Apis mellifera L., and myiasis, caused by this fly, is reported in several European, North African and Middle Eastern countries. Nevertheless, very little knowledge concerning the aggression and parasitisation behavior of S. tricuspis toward A. mellifera is available in the scientific literature, and the temporal pattern of aggression remains unclear. The aim of this investigation was to describe the aggressive behavior of S. tricuspis and to provide data on pupation and adult emergence in order to identify further tools for the control of senotainiosis in beekeeping. Data were collected in an apiary in Pisa province (Tuscany, Italy), where observations of aggressive behavior were conducted indirectly by using a VHS camera and also directly by an observer. Four behavioral categories of the attack were described. A total of 55 aggressions, 21 beecatchers, 104 chases and 6 parasitization events were recorded with the camera. Slow-motion recording analyses of the parasitization episodes resulted in contact of at least 1\/6 s between the parasitoid and the host. Through four days of direct observations, a total of 1633 aggression events were recorded. The daily temporal pattern of the number of aggressions showed two main peaks: one during the morning hours (i.e., from 10:00 to 11:00) and one in the afternoon (i.e., from 15:00 to 17:00). The morphometric data on the first-instars of S. tricuspis allowed us to hypothesize a penetration in the bee through its prothoracic spiracle as a modality of entrance in the host body. Third-instars successfully pupate when sinking in topsoil or clay soil, and adults emerge when left to a 4 \u00b0C overwintering period of six months. Furthermore, the high mortality rate of those larvae that did not sink and did not pupate successfully suggests that reaching a certain depth in the soil is a determining factor for larvae survival and that mulch and\/or minimum soil tillage could prevent severe senotainiosis in apiaries.<\/jats:p>","DOI":"10.3390\/insects14050415","type":"journal-article","created":{"date-parts":[[2023,4,27]],"date-time":"2023-04-27T02:18:34Z","timestamp":1682561914000},"page":"415","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Host-Parasitoid Relationship between Apis mellifera (Linnaeus, 1758) and Senotainia tricuspis (Meigen, 1838) (Diptera, Sarcophagidae): Fly Aggression Behavior and Infestation Rates of Senotainiosis"],"prefix":"10.3390","volume":"14","author":[{"given":"Gianluca","family":"Bedini","sequence":"first","affiliation":[{"name":"Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara Benedetta","family":"Boni","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy"},{"name":"Interdepartmental Centre of Agro-Environmental Research \u201cEnrico Avanzi\u201d, University of Pisa, Via Vecchia di Marina 6, 56122 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1571-3620","authenticated-orcid":false,"given":"Francesca","family":"Coppola","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy"},{"name":"Interdepartmental Centre of Agro-Environmental Research \u201cEnrico Avanzi\u201d, University of Pisa, Via Vecchia di Marina 6, 56122 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1592-7522","authenticated-orcid":false,"given":"Simona","family":"Sagona","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy"},{"name":"Department of Pharmacy, University of Pisa, Via Bonanno 6, 56126 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matteo","family":"Giusti","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mauro","family":"Pinzauti","sequence":"additional","affiliation":[{"name":"Italian Beekeeping Federation (FAI), Corso Vittorio Emanuele II 101, 00186 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0808-3037","authenticated-orcid":false,"given":"Antonio","family":"Felicioli","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy"},{"name":"Interdepartmental Research Centre \u201cNutraceuticals and Food for Health\u201d, University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,26]]},"reference":[{"key":"ref_1","first-page":"277","article-title":"Recherches sur la morphologie et la distribution g\u00e9ographique des Dipt\u00e8res \u00e0 larves parasites","volume":"Volume Tome II","author":"Lechevalier","year":"1941","journal-title":"Etudes sur le Mouches Parasites, Calliphorides Calliphorines (suite), Sarchophagines et Rhinophorines de l\u2019Europe Occidentale et M\u00e9ridionale"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2489","DOI":"10.1080\/00222933.2020.1854361","article-title":"Review of the genus Senotainia Macquart, 1846 (Diptera: Sarcophagidae) of the Middle East","volume":"54","author":"Verves","year":"2020","journal-title":"J. Nat. Hist."},{"key":"ref_3","first-page":"23","article-title":"Nuovo allarme: C\u2019\u00e8 una mosca che distrugge gli alveari!","volume":"23","author":"Pinzauti","year":"1996","journal-title":"Apitalia"},{"key":"ref_4","unstructured":"Guilhon, G. (1949, January 20\u201327). Apimyasis. Proceedings of the XIII International Beekeeping Congress, Amsterdam, The Netherlands."},{"key":"ref_5","first-page":"149","article-title":"Constatations sur la frequence des Myases apiares","volume":"97","author":"Rousseau","year":"1953","journal-title":"Apiculteur"},{"key":"ref_6","first-page":"33","article-title":"Censimento della presenza e del grado di infestazione di Senotainia tricuspis (Meigen) in Toscana","volume":"1\u20132","author":"Giusti","year":"2012","journal-title":"APOidea Anno IX"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Carpana, E., and Lodesani, M. (2014). Patologia e Avversit\u00e0 Dell\u2019alveare, Springer.","DOI":"10.1007\/978-88-470-5650-3"},{"key":"ref_8","first-page":"39","article-title":"Disa parazitoza n\u00eb blet\u00ebt tona","volume":"4","author":"Leka","year":"1986","journal-title":"Bul. Shk. Zootec. Vet."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1080\/00379271.2009.10697615","article-title":"Incidence and geographical distribution of honeybee (Apis mellifera L.) pests in Jordan","volume":"45","author":"Zaitoun","year":"2009","journal-title":"Ann. Soci\u00e9t\u00e9 Entomol. Fr."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1080\/00218839.2015.1099988","article-title":"Presence and infestation rate of Senotainia tricuspis (Meigen) (Diptera, Sarcophagidae) on honey bees in the Mediterranean Region","volume":"54","author":"Haddad","year":"2015","journal-title":"J. Apic. Res."},{"key":"ref_11","unstructured":"Loucif-Ayad, W. (2019, January 26\u201328). Biodiversity and honey bee diseases in Algeria. Proceedings of the International Biodiverstiy & Ecology Sciences Symposium (BioEco19), Istanbul, Turkey."},{"key":"ref_12","unstructured":"Hussein, M.H. (1997, January 1\u20136). Beekeeping in Sultanat of Oman. Proceedings of the 35th International Apimondia Congress, Antwerp, Belgium."},{"key":"ref_13","first-page":"539","article-title":"Larves de dipt\u00e9res endoparasites thoraciques de l\u2019abeille (Apis mellifica)","volume":"100","author":"Simintzis","year":"1949","journal-title":"Rev. Med. Vet."},{"key":"ref_14","first-page":"287","article-title":"La mouche Senotainia tricuspis Meig., agent probable de la maladie de la disparition qui attient les abeilles","volume":"281","author":"Mathis","year":"1975","journal-title":"Compter Rendus Ebd. Sci. Acad. Sci."},{"key":"ref_15","first-page":"119","article-title":"Notulae dipterologiche. Miltogrammini e Metopini (Dipt. Sarcophagidae) dell\u2019Italia Centrale","volume":"32","author":"Venturi","year":"1947","journal-title":"Redia"},{"key":"ref_16","first-page":"61","article-title":"Contributo alla conoscenza della Senotainia tricuspis Meig., Dittero Sarcofagide, endoparassita dell\u2019ape domestica","volume":"21","author":"Giordani","year":"1955","journal-title":"Boll. Ist. Entomol. Univ. Bologna"},{"key":"ref_17","first-page":"251","article-title":"Importanti studi in Sardegna su un parassita dell\u2019ape adulta","volume":"27","author":"Diana","year":"1950","journal-title":"Apic. Ital."},{"key":"ref_18","first-page":"4","article-title":"La Senotainia tricuspis (Meigen) (Diptera, Sarcophagidae) negli apiari della Toscana litoranea","volume":"16","author":"Santini","year":"1995","journal-title":"Ape Nostra Amica"},{"key":"ref_19","first-page":"3","article-title":"Sulla biologia e la possibilit\u00e0 di controllo della Senotainia tricuspis (Meig.) (Diptera, Sarcophagide) in apiari della Toscana","volume":"13","author":"Santini","year":"1996","journal-title":"Disinfestazione Ig. Ambient."},{"key":"ref_20","first-page":"179","article-title":"Recenti casi di \u201capimiasi\u201d da Senotainia tricuspis (Meigen) (Diptera, Sarcophagide) verif\u00eccatisi in Italia Centrale","volume":"86","author":"Pinzauti","year":"1995","journal-title":"Apic. Mod."},{"key":"ref_21","unstructured":"Hattoum, A. (1996, January 17\u201320). Senotainia tricuspis: A parasite of Syrian honey bees. Proceedings of the 1st International Arab Apicultural Congress, Beirut, Lebanon."},{"key":"ref_22","first-page":"673","article-title":"Presence and infestation of the parasitoid fly, Senotainia tricuspis (Meigen) (Diptera, Sarcophagidae) of honey bees in Sultanate of Oman","volume":"36","author":"Eshbah","year":"2016","journal-title":"Minia J. Agric. Res. Dev."},{"key":"ref_23","first-page":"69","article-title":"Senotainia tricuspis em Portugal","volume":"18","author":"Rocha","year":"1986","journal-title":"Repos. Trab. Lab. Nac. Investig. Vet."},{"key":"ref_24","unstructured":"Murilhas, A. (2009, January 3\u20134). Honey bee diseases and colony losses in Portugal. Results from the last nationwide survey. Proceedings of the IV Prevention of Honey Bee Colony Losses Conference, Faculty of Agriculture University of Zagreb, Zagreb, Croatia."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1080\/0005772X.2000.11099473","article-title":"A review of beekeeping in Arab countries","volume":"81","author":"Hussein","year":"2000","journal-title":"Bee World"},{"key":"ref_26","first-page":"4","article-title":"Dute Rivind Raspindizca bolitar molipsitoare so purasibare ull albinclor intara nonstron","volume":"8","author":"Pelimon","year":"1957","journal-title":"Apicoltura"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1080\/00218839.1981.11100498","article-title":"Observations on the morphology, relationships and ecology of Apis mellifera of Oman","volume":"20","author":"Dutton","year":"1981","journal-title":"J. Apic. Res."},{"key":"ref_28","unstructured":"Pajuelo, A.G., and Fernandez Arroyo, M.P. (1979, January 14\u201320). Las enfermedades de las abejas en Espana. Proceedings of the XXVII International Apicoltural Congress (Apimondia eds), Athens, Greece."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1051\/apido:19960605","article-title":"Prevalence of pasitization by Diptera in Apis mellifera L. in Southern Spain","volume":"27","year":"1996","journal-title":"Apidologie"},{"key":"ref_30","first-page":"304","article-title":"Larva of Senotainia tricuspis Meig. causing heavy losses of bees","volume":"24","author":"Boiko","year":"1939","journal-title":"Comptes Rendus Acad. Sci."},{"key":"ref_31","first-page":"43","article-title":"Myasis caused by larvae of Senotainia tricuspis in bees","volume":"6","author":"Smirnov","year":"1987","journal-title":"Veterinariya"},{"key":"ref_32","unstructured":"Bedini, G., Pinzauti, M., and Felicioli, A. (2006, January 25\u201327). Interaction between Apis mellifera and its parasites Senotainia tricuspis and Varroa destructor: A teoric model. Proceedings of the International Apicultural Scientific Conference, Pulawy, Poland."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Bailey, L., and Ball, B.V. (1991). Honey Bee Pathology, Academic Press. [2nd ed.].","DOI":"10.1016\/B978-0-12-073481-8.50006-0"},{"key":"ref_34","unstructured":"Boiko, A.K. (1958, January 15\u201323). Senotainiosis of bees. Proceedings of the XVII Congresso Internazionale di Apicoltura, Roma, Italy."},{"key":"ref_35","first-page":"863","article-title":"Senotainia tricuspis Meigen parasite larvaire de l\u2019abeille adulte (Apis mellifica)","volume":"144","author":"Simintzis","year":"1950","journal-title":"C. R. Seances Soc. Biol. Fil."},{"key":"ref_36","first-page":"25","article-title":"Mosca killer: Le osservazioni sul campo di un apicoltore","volume":"9","author":"Astolfi","year":"2000","journal-title":"Apitalia"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1163\/156853974X00534","article-title":"Observational study of behavior: Sampling methods","volume":"49","author":"Altman","year":"1974","journal-title":"Behavior"},{"key":"ref_38","unstructured":"Haccou, P., and Meelis, E. (1994). Statistical Analysis of Behavioural Data: An Approach Based on Time-Structured Models, Oxford University Press. [1st ed.]."},{"key":"ref_39","unstructured":"Chauvin, R. (1968). Traite\u00b4 de Biologie de l\u2019Abeille; Biologie et Physiologie Generales, Masson. [1st ed.]."},{"key":"ref_40","first-page":"8","article-title":"Senotainiosi e nomadismo apistico","volume":"12","author":"Pinzauti","year":"2006","journal-title":"Apitalia"},{"key":"ref_41","unstructured":"Pires, S., Cadavez, V., and Val\u00e9rio, M.J. (2011, January 21\u201325). Prevalence and geographical distribution of Senotainia tricuspis (Meigen). Diagnosis and Control of Bee Diseases. Proceedings of the Apimondia, Buenos Aires, Argentina."},{"key":"ref_42","first-page":"111","article-title":"Investigation on the presence in Latium of Senotainia tricuspis (Meigen) (Diptera Sarcophagidae), endoparasitoid of Apis mellifera L.","volume":"83","author":"Piazza","year":"2000","journal-title":"Redia"},{"key":"ref_43","unstructured":"Pinzauti, M., Giglioli, A., and Felicioli, A. (1998, January 11\u201313). Investigation on the presence of the dipterian Senotainia tricuspis (Meigen) (Diptera Sarcophagidae) in apiaries located in an inland area of central Tuscany (Italy). Proceedings of the Seventh Conference of the Italian Section of the International Union for the Study of Social Insects (IUSSI), Bologna, Italy."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1590\/S1519-69842003000100021","article-title":"Aphaereta sp.(Hymenoptera: Braconidae: Alysiinae) as a natural enemy to Peckia chrysostoma (Wiedemann)(Diptera: Sarcophagidae), in Brazil","volume":"63","author":"Marchiori","year":"2003","journal-title":"Braz. J. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"708","DOI":"10.11606\/issn.1678-4456.bjvras.2006.26582","article-title":"Gnathopleura quadridentata (Wharton) (Hymenoptera: Braconidae: Alysiinae) as natural enemy of Sarcodexia Lambens (Wiedemann)(Diptera: Sarcophagidae) in Brazil","volume":"43","author":"Marchiori","year":"2005","journal-title":"Braz. J. Vet. Res. Anim. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Marchiori, C.H. (2018, January 2). Natural enemies of Oxysarcodexia thornax (Walker) (Diptera: Sarcophagidae) collected in Brazil. Proceedings of the XXXII Brazilian Congress of Zoology (CBZ). Foz do Igua\u00e7u, Paran\u00e1, Brazil.","DOI":"10.32388\/519602"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1590\/S0074-02762001000600023","article-title":"Prey choice by facultative predator larvae of Chrysomya albiceps (Diptera: Calliphoridae)","volume":"96","author":"Faria","year":"2001","journal-title":"Mem. Inst. Oswaldo Cruz"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1023\/B:JOIR.0000028574.91062.18","article-title":"Cannibalistic behavior and functional response in Chrysomya albiceps (Diptera: Calliphoridae)","volume":"17","author":"Faria","year":"2004","journal-title":"J. Insect Behav."},{"key":"ref_49","first-page":"13","article-title":"Larves de Dipt\u00e8res du g\u00e9nre Senotainia parasites thoraciques internes de l\u2019abeille adulte","volume":"2","author":"Simintzis","year":"1949","journal-title":"Rev. Fran\u00e7aise Apic."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1080\/00218839.2004.11101119","article-title":"Differences in the morphology of prothoracic and propodeal spiracles in three strains of Apis mellifera: Possible relation to resistance against Acarapis woodi","volume":"43","author":"Hatjina","year":"2004","journal-title":"J. Apic. Res."},{"key":"ref_51","first-page":"11","article-title":"L\u2019impiego delle trappole cromotropiche nella difesa integrata delle colture: Stato attuale e prospettive","volume":"37","author":"Quaglia","year":"1988","journal-title":"Inf. Fitopatol."},{"key":"ref_52","unstructured":"Bedini, G. (2006). Indagine Sulla Relazione Ospite-Parassita Tra L\u2019Ape Eusociale Apis Mellifera L. (Hymenoptera, Apoidea) E IL Dittero Endoparassitoide Senotainia Tricuspis (Meigen) (Diptera, Sarcophagidae): Note Etologiche, Ecologiche Ed Applicative. [Master\u2019s Thesis, Facolt\u00e0 di Scienze Matematiche, Fisiche e Naturali, Corsi di Laurea in Scienze Biologiche, Universit\u00e0 di Pisa]."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/14\/5\/415\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:23:53Z","timestamp":1760124233000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/14\/5\/415"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,26]]},"references-count":52,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["insects14050415"],"URL":"https:\/\/doi.org\/10.3390\/insects14050415","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,26]]}}}