Diptera Attracted by the Truffle Tuber Aestivum Vittadini and by Dimethyl Sulphide in Sweden
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ISSN 0945-3954 Studia dipterologica 23 (1) 2016: 139–145 Diptera attracted by the truffle Tuber aestivum VITTADINI and by dimethyl sulphide in Sweden [Von der Trüffel Tuber aestivum VITTADINI und von Dimethylsulphid angelockte Zweiflügler in Schweden] by Ingemar STRUWE and Christina WEDÉN Uppsala (Sweden) Uppsala (Sweden) Abstract The ability of the truffle Tuber aestivum VITTADINI and of dimethyl sulphide, its volatile organic compound, to attract Diptera has been studied in the field in Sweden. Both the truffle and the compound were found to attract Heleomyzidae identically and exclusively, especially of the genus Suillia ROBINEAU-DESVOIDY. Flies of that genus indicated by their behaviour the locations of hypogeous truffles in nature. We conclude that dimethyl sulphide is the active compound attracting Diptera to T. aestivum in the field and that heleomyzid flies are specifically attracted. The main “truffle fly” in SwedenSuillia is pallida (FALLÉN, 1820), although other Suillia species as well as Tephrochlamys LOEW and Tephrochlaena CZERNY are involved. The mycetophilid Stigmatomeria crassicornis (STANNIUS, 1831) as well as the trichocerid Trichocera saltator (HArrIS, 1776) are also attracted by dimethyl sulphide. Key words Heleomyzidae, Suillia, Mycetophilidae, Stigmatomeria, Trichoceridae, Trichocera, Europe, Sweden, Truffle,Tuber aestivum, semiochemical, dimethyl sulphide Zusammenfassung Die Trüffel Tuber aestivum VITTADINI und Dimethylsulfid, einer ihrer flüchtigen organischen Inhaltsstoffe, wurden in Feld- versuchen in Schweden auf die Fähigkeit hin untersucht, Zweiflügler anzulocken. Sowohl die Trüffel als auch die chemische Verbindung erwiesen sich gleichermaßen und ausschließlich attraktiv für Heleomyzidae, insbesondere aus der Gattung Suillia ROBINEAU-DESVOIDY. Die Fliegen dieser Gattung zeigten durch ihr Verhalten natürliche Standorte hypogäischer Trüffel an. Daraus wird geschlussfolgert, dass Dimethylsulfid der aktive Inhaltsstoff ist, mit dem T. aestivum in der Natur Zweiflügler anlockt und dass die Substanz besonders attraktiv auf Heleomyzidae wirkt. Die bedeutendste „Trüffelfliege“ in Schweden ist Suillia pallida (FALLÉN, 1820), obwohl auch andere Arten von Suillia als auch von Tephrochlamys LOEW und Tephrochlaena CZERNY beteiligt sind. Die Pilzmücke Stigmatomeria crassicornis (STANNIUS, 1831) sowie die Wintermücke Trichocera saltator (HArrIS, 1776) werden auch von Dimethylsulfid angezogen. Stichwörter Heleomyzidae, Suillia, Mycetophilidae, Stigmatomeria, Trichoceridae, Trichocera, Europa, Schweden, Trüffel, Tuber aestivum, Botenstoff, Dimethylsulfid Introduction The truffle fungus Tuber aestivum VITTADINI is widely distributed in Europe. Its most northern known locality is the Baltic island Gotland, Sweden (WEDÉN 2004). Since the late 1990s, scientific knowledge and public aware- ness of the natural distribution of truffles in Sweden has developed and also caught increasing interest from those involved in Scandinavian gastronomy. A market for truffles has been established in Sweden since then, involving truffle hunting with trained dogs in the wild and truffle cultivation (WEDÉN et al. 2009). A Swedish truffle hunter noticed the presence of hovering flies in spots where she would also find truffles (Eva PETTERSSON, pers. comm.). After learning about the French method of finding mature specimens of truffles by observing the © Senckenberg Gesellschaft für Naturforschung, 2017 139 Struwe & Wedén: Diptera attracted by the truffle Tuber aestivum and by dimethyl sulphide hovering behaviour of certain flies on the ground, she started to use this method successfully to find mature truffle specimens in her local truffle grounds. A truffle is a fungal life-form defined by its hypogeous fruiting bodies. The ability of active spore dispersal has been lost so the fungus is instead dependent on animal spore vectors, perhaps including insects. At full spore maturity, truffle fruiting bodies emit an array of volatile organic compounds (VOCs) that attract mammals such as mice, squirrels and boars to unearth and eat them. The spores are then efficiently spread in faecal pellets (TRAppE & CASTELLANO 1991). The truffle life-form has developed multiple times in fungi (TRAppE et al. 2001), and volatile and non-volatile components are being studied to understand the nature of the fungus-animal interactions. Truffle VOCs have shown potential for interaction with animals, plants, other fungi and bacteria (SPLIVALLO et al. 2011). Due to the gastronomic, and hence economic, interest in certain Tuber spp., most studies on truffle VOCs have been done on species belonging to this genus in the Ascomycota (SPLIVALLO et al. 2011). Although common in many species, the relative quantities of VOCs give each truffle species a unique, species-specific scent at full spore maturity. The characteristic aroma of mature Tuber fruiting bodies is to a large extent due to small molecules, often sulphur-containing hydrocarbons, often comprising alcohol, aldehyde and/or ketone functional groups (SPLIVALLO et al. 2011). In T. aestivum, the most prominent compounds producing its scent, as identified by gas chromatography – mass spectrometry (GC-MS) of headspace solid-phase microextraction, are dimethyl sulphide, 2-methyl propanal, 2-methyl butanal, 3-methyl butanal, 2-methyl-1-propanol, 2- methyl-1-butanol and 3-methyl-1-butanol (DÌAZ et al. 2009). CULLERÉ et al. (2010) on the other hand, used GC-olfactometry to identify the VOCs most important to the human perception of the aroma of T. aestivum, and these were dimethyl sulphide, dimethyl disulphide, methional, 3-methyl-1-butanol, 1-hexen-3-one and 3-ethylphenol. Although similarities exist between the two studies, the differences in identified compounds are evident and may be accounted for by the specific sensitivity of the human nose to sulphur-containing VOCs. In the middle of the 19th century GOUREAU (1852) and LABOULBÈNE (1864) respectively reared insects from truffles and identified a list of the Diptera in truffles which was little changed for the next hundred years. They verified the fly family Heleomyzidae and its genusSuillia as important members of the truffle-associated fauna. HACKMAN & MEINANDER (1979) in Finland widened the perspective by rearing Diptera from non-hypogeous macrofungi and found that the genus Suillia was richly represented even there. BRATEK et al. (2001) reared insects from truffle sporocarps in Hungary and identified beetles and flies mainly to family level. Again the heleomyzid genus Suillia was strongly numerically dominant, especially Suillia pallida (FALLÉN, 1820). The genus Suillia seemed to have a specificity for Tuber species, as it was not reared from any other truffle genus. Rearing records in Britain of Suillia humilis (MEIGEN, 1830), S. pallida, S. affinis (MEIGEN, 1830) and Suillia variegata (LOEW, 1862) from truffles were reported inC HANDLER (2010). Suillia species also became commonly known among Central European truffle hunters as “the truffle fly”, but scientific confirmation of this is still lacking (CHANDLER 2010). Field studies in Sweden (TJERNBY 2003) designed for spore dispersal research revealed Suillia species in some traps baited with the truffle Tuber aestivum, but no further identification was made. GArcÍA-MONTERO et al. (2004) in Spain sampled flies by netting in habitats with known high abundance of the truffle Tuber mesentericum VITTADINI and identified them all as Suillia gigantea (MEIGEN, 1830), a species also frequent in truffle regions in France C( OUTIN 1989). TALOU et al. (1990) studied the ability of a number of VOCs from truffles Tuber( melanosporum VITTADINI) to attract mammals such as dogs and pigs; the only buried sample reliably localized contained dimethyl sulphide (DMS). PACIONI et al. (1991) tested the attracting ability of different truffle VOCs and found that DMS was superior in attracting insects. Identification was however only made to order level in Diptera and family level in Coleoptera. In an excellent research review SPLIVALLO et al. (2011) stated that in order to confirm that DMS is the actual attractant in nature, behavioural assays with real truffles should be conducted. Aim of study We designed a study in order to identify the fly species attracted by T. aestivum in nature in Sweden, and to evaluate the role of DMS in attracting flies under field conditions. Comparing the fly fauna attracted by DMS 140 Studia dipterologica 23 (1) 2016: 139–145 traps and truffle traps, we would try to find further evidence that DMS is the active semiochemical of truffles. Through field observations, we wanted to identify fly species with verified truffle-indicating behaviour. Materials and methods The study was conducted on the Baltic island Gotland in areas with well-known high abundance of T. aestivum during two separate weeks in autumn 2014: late September and early November. In addition the third activity below was performed during October. These calendar periods were chosen to reflect expected higher fly activity and truffle maturation, respectively. Four different activities were performed. 1. Sealed 10 litre plastic boxes with a narrow funnel entrance (Fig. 1) were placed in the terrain in two separate lines 200 metres apart, 10 boxes in each line and 50 metres between each box. In one line the boxes were baited with fresh mature truffle, and in the other line with partly sealed tubes containing DMS. The boxes were emptied daily and the entire yield preserved and morphologi- cally identified using the keys in BEUK (2012),