Insect-truffle interactions – potential threats to emerging industries?

Abstract

Truffle harvests are declining in Europe, due to droughts, and this offers an opportunity for production to be developed in countries such as the UK and Poland, where rainfall tends to be higher. Drier Mediterranean summers seem to be associated with a decrease in the harvest of the Périgord truffle (Tuber melanosporum) in Spain, France and Italy. However, other species, for example the Burgundy truffle (Tuber aestivum) offer opportunities for production in the more temperate environments north of the Alps. Truffles across Europe can be infested by insect larvae, seriously reducing their economic and culinary quality. Here, using a combination of literature sources and a field survey, we present a commentary on insects attacking truffles, aiming to highlight those species that could be potential pests in the British and Polish emergent industries. There is a remarkable disparity in coincidence of records of insects and truffles in these countries, yet a survey in Poland confirms that insects can be abundant. We discuss reasons for this disparity and suggest that biochemical methods could easily be developed for detection of the truffles and their attackers.

Introduction

Truffles are hypogeous fungi belonging to the Pezizales, mostly in the genus Tuber, and comprise a large group of ectomycorrhizal fungi growing in symbiosis with the roots of several vascular plant species (angiosperms and gymnosperms). The fruit body of these fungi is a subterranean complex apothecium, commonly known as the truffle. The geographic distribution of truffles mainly covers the temperate zones of the Northern Hemisphere, with at least three areas of genetic differentiation in Europe, South East Asia and North America (Pomerico et al., 2006). So far, seven species of Tuber have been reported from Poland, namely Tuber mesentericum (Ławrynowicz, 1999), Tuber aestivum, Tuber excavatum, Tuber rufum (Hilszczańska et al., 2008), Tuber maculatum (Ławrynowicz, 2009), Tuber macrosporum (Hilszczańska et al., 2013) and Tuber brumale (Merényi et al., 2014). According to the Fungal Records Database of the British Isles (http://www.fieldmycology.net/FRDBI/FRDBI.asp) all 7 species have been recorded in the UK, though none have many attributed records. That with the most is T. aestivum with 110 records, but to put this into perspective, the fungal species with the most records (Hypholoma fasciculare) has 16,259 (as of 21 September 2016).

Economically, truffles are the most valuable non-timber products of forest ecosystems, and are highly prized for their culinary qualities in countries such as France, Italy and Spain. Highly desirable truffles (i.e. Tuber magnatum (white) or Tuber melanosporum (black)) may attract remarkable prices, of around €2000–€3000 kg⁻¹, with the industry in Italy worth around €400 million per annum (Büntgen et al., 2012, Pieroni, 2016). This may be the primary reason why a truffle industry is emerging in countries such as the UK and Poland. However, it may also be due to the decline of harvests of the highly-prized black truffle (T. melanosporum) in its main habitats due to increased frequency of droughts (Büntgen et al., 2011, Büntgen et al., 2012, Büntgen et al., 2015). Although neither T. magnatum nor T. melanosporum have been found in the UK or Poland, two other species (T. aestivum and T. brumale) are commercially traded in countries such as Spain and Hungary (Stobbe et al., 2013; Martin-Santafe et al., 2014). Indeed, recent evidence suggests that T. aestivum in particular may be found in suitable areas north of the Alps, such as Germany, and even as far north as southern Sweden and Finland (Stobbe et al., 2012, Stobbe et al., 2013). The first cultivated specimen of T. aestivum was found in England in March 2015 (http://www.bbc.co.uk/news/science-environment-31826764) and in Wales in July 2016 (http://www.itv.com/news/wales/2016-07-25/first-ever-cultivated-truffle-harvested-in-wales/). In Poland, three truffle orchards (with T. aestivum) have been established and maintained by the Forest Research Institute, one of which is productive (Hilszczańska et al., 2008, Hilszczańska and Sierota, 2010, Hilszczańska, 2016). Therefore, there is great economic potential for the emergent industries in more northerly countries to fill gaps in the European market, and it is timely to identify any problems that might reduce their potential in future.

Ecologically, these fungi are of considerable importance because of the benefits of the mutualistic association they provide to their host plants (Pacioni and Comandini, 1999). In addition, the relatively long-lived fruit body provides a food source for invertebrates and vertebrates (Johnson, 1996, Blackwell, 2005). Some species of truffles, e.g. T. magnatum, T. melanosporum and T. aestivum, have a high culinary value because of their aroma (Mello et al., 2006) and in natural habitats, the volatiles produced are essential for attracting animals that spread the spores (Fogel and Trappe, 1978). However, some animals have evolved a capacity for feeding on truffle sporophores. These belong to various taxonomic groups and are termed ‘hydnophagous’ (Pacioni, 1989), from Greek ‘hydnon’, truffle, and ‘phagous’, eating. For certain animals, such as mammals (rodents, deer, boars), birds and slugs, truffles are a valuable part of their diet (Johnson, 1996, Vernes et al., 2015), yet for several species or genera of arthropods, mainly in the Coleoptera and Diptera, the fungi may represent their complete diet (Pacioni et al., 1995, Di Santo, 2013). Indeed, there is much anecdotal evidence that truffles may be discovered by searching for the flies that oviposit within the fruit body, though this is a laborious and unpredictable procedure (Blackwell, 2005). Scattered through the literature are occasional reports of truffle sporocarps being infested by insect larvae, thus reducing their marketable value considerably (Ciampolini and Suss, 1982, Martin-Santafe et al., 2014). Our aim here is to provide a survey of the insects that may be associated with truffles in two countries, which as well as being ecologically interesting, highlights potential problems for the emerging truffle industry.