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Exploring the involvement of honey bee pathogens in colony collapses from epidemiological data, pathogen genotyping and host immune responses. Jorgen Ravoet Promotor: Prof. Dr. Dirk de Graaf Academic year 2014-2015 Thesis submitted in fulfilment of the requirements for the degree of Doctor in Sciences: Biochemistry and Biotechnology Department of Biochemistry and Microbiology Supervisors Promotor: Prof. Dr. Dirk de Graaf Laboratory of Molecular Entomology and Bee Pathology (L-MEB) Department of Biochemistry and Microbiology Faculty of Science, Ghent University, Belgium Examination committee Prof. Dr. Savvas Savvides (Ghent University, Belgium, chairman) * Prof. Dr. Dirk C. de Graaf (Ghent University, Belgium, secretary) * Prof. Dr. Guy Smagghe (Ghent University, Belgium) * Prof. Dr. Peter Geldhof (Ghent University, Belgium) * Prof. Dr. Tom Wenseleers (KU Leuven, Belgium) * Prof. Dr. Peter Neumann (University of Bern, Switzerland) * Dr. Bach Kim Nguyen (University of Liege, Belgium) * Dr. Lina De Smet (Ghent University, Belgium) * Members of the reading committee Dean: Prof. Dr. Herwig Dejonghe Rector: Prof. Dr. Anne De Paepe The author and the promotor give the permission to use this thesis for consultation and to copy parts of it for personal use. Every other use is subject to the copyright laws, more specifically the source must be extensively specified when using results from this thesis. Please refer to this work as: Ravoet, J. (2013) Exploring the involvement of honey bee pathogens in colony collapses from epidemiological data, pathogen genotyping and host immune responses. PhD thesis, Ghent University. Funding: This study was financially supported by Research Foundation-Flanders (FWO) (research Grant G.0628.11). Author’s email address: [email protected] Front cover Drawings: Kathleen Hamaekers DANKWOORD Ongelooflijk wat er allemaal kan gebeuren op enkele jaren tijd. Vier jaar geleden kwam ik vol zenuwen op sollicitatiegesprek bij prof. Dirk de Graaf. Na enkele dagen kreeg ik het verlossende telefoontje dat ik was aangenomen. Nu kan ik met veel voldoening terug kijken op de periode sindsdien, met goede en helaas ook slechte tijden. Dit alles zou echter niet mogelijk zijn geweest zonder vele personen. In de eerste plaats dank ik mijn promotor prof. Dirk de Graaf voor het vertrouwen, de steun en het gebruik van het onderzoekslabo. Ik zou zelf niet willen opdraaien voor alle offertes die ik op al die jaren met succes aan hem heb voorgesteld. Ook prof. Tom Wenseleers heeft als promotor van het FWO project ‘Deformed wing virus: a contributory factor of Colony Collapse Disorder in honeybees?’, waarop ik vier jaar betaald ben, een belangrijke bijdrage heeft geleverd. Vanzelfsprekend is het FWO dan bedankt voor de financiële steun die dit doctoraat mogelijk heeft gemaakt. Alle coauteurs van de verschillende hoofdstukken delen in mijn dank. Hun bijdragen waren dikwijls niet te onderschatten, en gaven de artikels mee vorm. Especially the efforts of Prof. Jay D. Evans and Dr. Ryan Schwarz to include us in their study of honey bee trypanosomatid taxonomy are much appreciated. This collaboration led to many fruitful discussions. Also Prof. Mariano Higes and Dr. Raquel Martin-Hernandez are thanked to allow a visit to their laboratory and to introduce me into experimental infections of Nosema ceranae. Vanzelfsprekend wil ik ook de grote rol van mijn vriendin Els in de verf zetten. Ze toont steeds begrip voor de lange werkuren, de jaarlijkse congressen in het buitenland en de klachten in mindere periodes. Sinds kort kunnen we ons samen toeleggen op de zorgen van onze schattige tweeling, Lars en Nore. Dit resultaat zou er natuurlijk nooit geweest zijn zonder de steun van familie en vrienden. Ik wil dan ook graag mijn ouders, grootouders, zus, toekomstige schoonbroer en schoonouders bedanken. Verder bedank ik de collega’s van het Laboratorium voor Moleculaire Entomologie en Bijenpathologie voor het aangename gezelschap en de leuke werksfeer. Marleen, bedankt voor alle bestellingen, de mede-doctoraatsstudenten Ellen D, Ellen F, Matthias en Tine (bovendien mijn voormalige thesisstudente) voor de toffe gesprekken tussen de experimenten door, Lina voor de begeleiding in het labo, de vele besprekingen en het beantwoorden van een constante stroom aan vragen. Ook Dieter, waarmee ik het genoegen had om een bureau te delen, zal ik zeker nooit vergeten. Het personeel van het informatiecentrum van bijenteelt waren ook dikwijls een grote hulp. Jeroen, Mikalai, Dries, Wilfried en Patrick, van harte bedankt om vaak honingbijen ter beschikking te stellen. Om af te sluiten wil ik nog graag alle leden van de jury bedanken voor hun opmerkingen die deze de eerste versie van doctoraatsthesis verder verfijnd hebben tot dit finale resultaat. SUMMARY Pollination is required for the cultivation in an agricultural context of many fruit, nut, vegetable and crops. European honey bees (Apis mellifera) are considered the most economically valuable pollinators for crop monocultures worldwide, followed by bumble bees (Bombus spp.). However, over the last decade unusually high honey bee colony losses have been reported. Several factors contribute to their decline, of which pathogens are the main culprits. We could confirm the presence of several parasites which were previously not known for Belgium. This included viruses (ALPV strain Brookings, AmFV, LSV and VdMLV), trypanosomatids (Crithidia mellificae and Lotmaria passim) and parasitic flies (Apocephalus borealis). Other pathogens were already reported from Belgian bumble bees, namely the neogregarine Apicysis bombi and the bacteria Spiroplasma apis and Spiroplasma melliferum, but remained ignored so far in honey bees. In this work, the pathosphere of Apis mellifera was extensively exploited. After the initial examination, we selected a few parasites for further characterisation. Our knowledge about most of these novel or neglected parasites is limited. For instance only few nucleotide sequences are available for some of them, such as A. bombi, A. borealis and AmFV. The transmission routes are also not yet known. Nevertheless, vertical transmission was proved for the viruses ALPV strain Brookings, LSV and VdMLV since we detected them in honey bee eggs. This demonstrates a vertical transmission, in accordance with previous studies on other viruses. Numerous of these pathogens were also discovered in solitary bees, caught nearby an apiary. Although solitary bees can suffer from honey bee parasites, as demonstrated for DWV and Nosema ceranae, spillover appears to occur in both direction. Indeed we detected SBV solely in solitary bees and not in honey bees. Nevertheless, solitary bees can also be infected by their specific pathogens. For the moment only microsporidians and fungi are known. The poor knowledge about some pathogens is demonstrated in this work since we could demonstrate that at least two trypanosomatids can infect honey bees and the presence of several novel LSV genotypes. Comprehensive characterisation revealed that a broad complex of related LSV genotypes exists in honey bees. We were able to assemble almost the entire genome of four LSV strains and observed high strain diversity. Moreover, we could demonstrate several strains within single bee specimens. Soon after its initial report in the USA, LSVs were reported from other countries and even from other hosts. The negative strand intermediate, a marker for replication of ssRNA (+) viruses, was also detected in honey bees and the mason bee Osmia cornuta. Also replication of ALPV strain Brookings and VdMLV in honey bees was demonstrated for the first time, besides LSV replication in the solitary bee O. cornuta. Concluding, during this work it became clear that honey bees face more parasites, and in particular more viruses, than previously thought. SAMENVATTING Honingbijen worden wereldwijd ingezet voor de bestuiving van allerlei fruit en gewassen. De laatste decenia worden echter ongewoon hoge kolonie sterftes waargenomen op verscheidene continenten zonder een eenduidige oorzaak. Ook de Belgische bijenkolonies worden jaarlijks hard getroffen. Verschillende oorzaken dragen bij aan deze sterftes, maar vooral de bijenpathogenen spelen een belangrijke rol. In dit doctoraatswerk zijn een breed gamma aan pathogenen onderzocht in Belgische bijenkolonies. Dit leidde tot de ontdekking van parasieten die nog niet eerder vermeld werden voor België, waaronder virussen (ALPV stam Brookings, AmFV, LSV en VdMLV), trypanosomen (Crithidia mellificae en Lotmaria passim) en parasitaire vliegen (Apocephalus borealis). Sommige andere gevonden pathogenen werden al eerder in Belgische hommels gedetecteerd, zoals de neogregarine Apicystis bombi en de bacteriën Spiroplasma apis en Spiroplasma melliferum. Tot nu toe werden ze echter verwaarloosd als honingbij parasieten. De pathosfeer, het totale scala aan pathogenen die de honingbij infecteren, werd in dit doctoraatswerk grondig bestudeerd. Na prevalentie onderzoeken in verscheidene stadia selecteerden we aan aantal van hen om verder te karakteriseren. Onze kennis is immers beperkt wanneer het gaat om een aantal verwaarloosde of nieuw ontdekte soorten. De manieren waarop deze zich verspreiden is ook niet goed gekend. Zo konden we de virussen ALPV stam Brookings, LSV en VdMLV aantonen in honingbij eitjes, wat dus verticale transmissie aantoont. Velen van de honingbij pathogenen werden eveneens aangetoond in solitaire bijen die we in de buurt van een bijenstand collecteerden. Voor een aantal parasieten zoals DWV en Nosema
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  • Zoologischer Anzeiger

    Zoologischer Anzeiger

    ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Zoologischer Anzeiger Jahr/Year: 1911 Band/Volume: 38 Autor(en)/Author(s): Sokolow Iwan Artikel/Article: Liste des Grégarines décrites depuis 1899a. 304-314 © Biodiversity Heritage Library, http://www.biodiversitylibrary.org/;download www.zobodat.at 304 5. Liste des Grégarines décrites depuis 1899a. ParB. Sokolow, St. Pétersbourg. eingeg. 10. Juni 1911. B. Subordre Schizogrégariues (Léger). [= Amoebosporidia Sehn.] 1900. Léger: G. R. Soc. Biol. T. LU. p. 868—870. Multiplication schizogonique. Fécondation isogame. Un ou plu- sieurs sporocystes. Différenciation des familles: Schizogonie extracellulaire. Conjugaison isogame. -— I. fana. Ophryo- cystidae. Schizogonie extracellulaire. Conjugaison anisogame. — II. fam. Schizo- cystidae. Schizogonie intracellulaire. Sporocystes à 4 sporoz. — III. fam. Sele- nidiidae. Changement d'hôte. Reproduction sexuelle anisogame. — IV. fam. Aggrégatidées. I. Fam. Ophryocystidae (Léger et Duboscq). 1908. Léger et Duboscq: Arch. f. Protistke. Bd. XII. S. 44—108. 1909. Léger et Duboscq: Arch. f. Protistke. Bd. XVII. S. 19—135. Gen. Ophryoeystis (Schneider). Schizontes de forme conique fixés à l'épithélium par de nombreuses radicelles. Un seul sporocyste octozoïque. 1) O. schneiden (Léger et Hagenmüller). 1900. Léger et Hagenmüller: Arch. Zool. Exp. (3). T. VIII. p. 40—45. 1907. Léger: Arch. f. Protistke. Bd. VIII. S. 159-203. Schizontes grégarinoïdes avec 1 à 4 noyaux, de forme conique; pas de schizontes mycétoïdes. Gamontes ovoïdes de 10 à 11 X 8 ,"• Cou- ples ovoïdes, allongés de 16 à 18 X ? /'> ave c une très mince enveloppe. Sporocystes biconiques de 11 sur 5,5 (a. Tubes de Malpighi de Blaps magica.