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Ecology of Spider Parasitoids: Koinobiont Ectoparasitoids From PALACKÝ UNIVERSITY OLOMOUC Faculty of Science Ecology of spider parasitoids : koinobio nt ecto parasitoids from Polysphincta genus group (Ichneumonidae, Ephialtini) Habilitation thesis in Ecology M.Sc. Stanislav Korenko, Ph.D. Prague 2017 Stanislav Korenko Habilitation thesis Content Content 2 1 Introduction 4 2 Structure of habilitation thesis 5 3 Parasitoids of spiders 6 3.1 Nematode and dipteran parasitoids associated with spiders 6 3.2 Hymenopteran parasitoids of spiders 6 3.3 Parasitoid wasps from the Polysphincta genus group (Ephialtini) 7 4 Life cycle and phenology of polysphinctine parasitoids 7 5 Host association 9 5.1 Host association of the genus Zatypota 10 5.1.1 European species of Zatypota 11 5.1.2 Oligophagy in Australian Zatypota kauros 12 5.2 Host association of Sinarachna pallipes and Polysphincta spp. 13 5.3 Host association of the genera Acrodactyla and Megaetaira in Europe 14 5.4 Host association of Reclinervellus nielseni across the Palearctic 15 5.5 Divergence in host association within genus Eriostethus 15 6 Behavioural manipulation of spider hosts 16 6.1 Host utilisation of Zatypota wasps 17 6.1.1 Zatypota wasps associated with theridiid spiders 17 6.1.2 Zatypota anomala associated with dictynid spiders 18 6.1.3 Zatypota picticollis associated with araneid spiders 18 6.1.4 Australian oligophagous Zatypota kauros 18 6.2 The specificity of host utilisation in the genera Acrodactyla and Megaetaira 18 6.3 The Reclinervellus nielseni parasitoid of Cyclosa spiders in the Palearctic 19 6.4 Three - dimensional cocoon webs of Polysphincta spp. and Sinarachna pallipes 20 in Europe 6.5 Divergence in host utilisation within the genus Eriostethus 21 7 Acknowledgements 21 8 References 22 9 List of supplements 29 Supplements 1 – 15 Author’s publications included in habilitation thesis Supplement 16 Corresponding author’s statement in connection to the habilitation thesis 2 Stanislav Korenko Habilitation thesis © S. Korenko, 2017 3 Stanislav Korenko Habilitation thesis 1 Introduction The p resented habilitation thesis deals with ecolog y of various parasitoid taxons associated with spider hosts (Araneae). My research over the last decade was focused on paras itoid ecology and host - parasitoid interactions including parasitoid life history, phenology, host range, host shift, host behavioural manipulation , and evolution of host utilisation. I studied various parasitoid groups associated with spiders , including small headed flies (Acroceridae) families (Kehlmaier et al. 2012) and wasps from Eupelmidae and Cryptinae (Ichneumonidae) (Korenko et al. 2013 ) , but my main researc h into spider host - parasitoid interaction s was conducted on wasps from the Polysphincta genus group ( Ichneumonidae, Ephialtini ). Most papers of mine concern wasps from the Polysphincta genus group (Ichneumonidae, Ephialtini ) , whose taxonomy is relatively well documented in Europe ( e.g. Fitton et al. 1987 ; 1988 ; Zwakhals 2006 ; Fritzén , Shaw 2014) ; however, their ecology and interaction s with spider hosts has been little studied. Initial work on their ecology and behaviour was done by Nielsen (e.g. 1923, 1928, 1929, 1935, 19 37) but essential studies were conducted only in the last decade (e.g. Belgers et al. 2013 ; Bovee, Leech, 2014 ; Fritzén 2010, 2014 ; Fritzén , Fjellberg 2014 and the studies presented here as part of this habilitation thesis). My first encounter with polysphinctine parasitoids was during my Ph.D. project , in wh ich I studied the biological control potential of spiders in apple orchards in Brno . I was surprised to find my first parasitoid larvae on spiders’ abdomens and I wondered what the se creatures were. I reared them in the laboratory and it was i dentified as Zatypota percontatoria ( Müller, 1776) . I still use this relatively common species as a model organism for various behavioural studies. From th at time , the interaction s between polysphinctine parasitoids and spiders became one of my main research interest s, and my first results were included in my Ph.D. thesis (Korenko 2010) . Nowadays I study the ecology of polysphinctine parasitoids in several parts of Eu rope. My collaboration with Dr. Kamil Holý from the Crop Research Institute, p rof. Stano Pekár from Masaryk University , and other colleagues from communities of Czech arachnologists and hymenopterologists was fruitful and resulted in several manuscripts wh ich have already been published, have been accepted for publication, or are in preparation. In Slovakia, I have collaborated for several years with M .S c. Martin Štefánik from Trenčianské Museum on the study of habitat preference and on collecting live para sitoids and their hosts for behavioural studies in the laboratory. The d istribution and ecology of rare polysphinctines are investi gated in collaboration with M .S c. Ľudmi la Černecká and Dr. Ivan Mihál from the Slovak Academy of Science at Zvolen. Polysphinctines are distributed sparsely and the parasitism rate is mostly low, between 0 – 2 % in Central Europe. Therefore, the collaboration with colleagues in the field and help with the collection of specimens and data on distribution is essen tial for my behavioural studies. In 2009, I began to investigate spider parasitoids in ecological farms and forest habitats in northern Italy (Piemonte) in collaboration with Dr. Marco Isaia from 4 Stanislav Korenko Habilitation thesis Università di Torino . Our fruitful collaboration is still running. Most of my behavioural studies were performed on individuals collected in northern Italy because the parasitism rate there is much higher (often above 10%) in comparison with localities in the Central Europe ( Korenko unpubl. data ) . Other important collaborations on resolving taxonomical and ecological issues have been conducted with Dr. Seraina Klopfstein from the Institute of Ecology and Evolution at Universität Bern in Switzerland, Kees Zwakhals from the Netherland s , Filippo Di Giovanni from Sapienza University of Rome in Italy, Dr . Keizo Takasuka from Keio University in Japan, p rof. William G. Eberhard from the Smithsonian Tropical Research Institute in Panama, Dr . Marcelo O. Gonzaga from Universidade Federal de Uberlândia , and Dr . Thiago G. Kloss from Univers idade Federal do Espírito Santo in Brazil , as well as several other colleagues from various parts of the world. In 2013, c ollaboration also began with p rof. Gimme Walter from Queensland University, which hosted me in their lab oratory during a stay in Australia . Some of our unique findings on the ecology of Australian spider parasitoids are discussed in the presented habilitation thesis ; others are being acquired . Recently , I have been working on an understanding of the evolution of host utilisation among polysphincitine wasps using a combination of molecular, morphological , and behavioural data in collaboration with most of above mentioned colleagues. The p resented habilitation thesis consist s of fourteen articles an d manuscripts in which I was the corresponding author and to which my contribution was between 40 - 100 %. One article has a different corresponding author and my contribution to the work was 25% (see Correspondence author’s statement in S upplement 16 ). 2 Structure of habilitation thesis The p resented thesis is a review of my published resea rch on the ecology of spider parasitoids from 2011 to the present. One article deals with dipteran endo parasitoids an d the other eleven with ichneumonid parasitoids , especially with wasps from the Polysphincta genus group (Ephialtini). The first chapter is a brief summarisa tion of knowledge on the ecology of the most important spider parasitoids . The n ext three chapters are concentrated on several aspects of the ecology of wasps from the Polysphincta genus group: 1) life history and phenology , 2) host association , and 3) the behavioural manipulation of spider hosts . Each chapter is a short summary of knowledge on the particular t opic and includes my own results. The f inal section consists of a list of articles which are included in the thesis, references , and supplements . The full texts of articles are included. 5 Stanislav Korenko Habilitation thesis 3 P arasit o ids of spiders The most important parasites and parasitoids associated with spider hosts belong to the order Hymenoptera, follow ed by Diptera and Nematode s ( e.g. Godfray 1984 ; Fitton et al. 198 7 ) . 3. 1 Nematode and dipteran parasitoid s associated with spiders Nematode parasites associated with spider hosts known from nature are restricted to the family Mermithidae (Poinar 1987). Mermithids were found parasitizing spiders of several families from araneomorph spiders ( the families Gnaphosidae, Anyphaenidae, Thomisidae, Sa lticidae, Linyphiidae, and Araneidae ( e.g. Poinar , Benton 1986) ) and several families of mygalomorph spiders (the families Ctenizidae, Dipluridae , and Migidae ( e.g. Poinar, Early 1990) ) . Dipteran parasites and parasitoid s associated with spiders are restricted to a few families and vary considerably in the mode of host utilization ; for example, some are egg predators , while others are endoparasitoids (e.g. Schlinger 1987), or even ectoparasitoid s (Schlinger et al. 2013). Several dipter an families – Dr osophilidae, Chloropidae, Phoridae and Sarcophagidae – are known to be predator s of spider eggs , while only Acroceridae and Tachinidae are considered to be true parasitoids of spiders. The most detailed host range has been documented for the genus Ogcodes , with about 40 host - parasite relationships
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