Associations between carabid beetles and fungi in the light of 200 years of published literature

One of the striking features of the Anthropocene is a rapid degradation of natural ecosystems^1,2, and an alarming decline of many species, which ultimately may lead to extinctions^3,4,5. Whereas conserving ecosystem functions is increasingly recognised as a vital need for humans^6,7,8, the interspecific interactions underpinning these functions are poorly understood^9,10. However, conserving such interactions can be particularly important when taxa providing high-value ecosystem services are involved^10,11.

Ground beetles (Coleoptera: Carabidae) have been long known for their benefits in agroecosystems^12,13. They play an important role in suppressing pests¹⁴, but several carabid species also consume seeds of herbaceous plants, making them a valuable asset for weed control as well¹⁵.

Fungi are also of vital significance in most of the world’s terrestrial ecosystems¹⁶. Mycorrhizal fungi improve nutrient uptake by a large range of plant species through intimate and specialised associations¹⁷, other fungi play a crucial role in decomposition¹⁸, and yet others are pathogens of both crops and pests in agroecosystems¹⁹. Fungal parasitism is one of the crucial agents of evolution²⁰.

Fungi and carabids often co-occur, and they can potentially interact in many ways. The soil environment carabids often inhabit is a reservoir of fungal propagules where the beetles can feed on spores, hyphae or fruiting bodies²¹. They may also be responsible for dispersal of spores of certain fungi²². Several parasitic or entomopathogenic fungi are in an obligatory relationship with their beetle hosts²³, therefore, the population decline of a ground beetle species could potentially lead to overlooked extinction cascades²⁴. However, our knowledge of the fungal-carabid interactions is still limited concerning the frequency of these interactions and on how their exact nature affect the parties involved. Indeed, we do not even have a catalogue of the carabid-fungi interactions, and they have not yet been organized into a comprehensive database. Such a database would be of particular importance from an integrated pest management point of view because both fungi and carabids can deliver ecosystem services, but how their interactions, and potential synergies or antagonisms, influence the delivery of these services is poorly understood.

In order to have a detailed overview of the interactions between Carabidae and the fungal kingdom, we collated a database containing previously reported associations between these taxa. Carabid and fungal species involved in the interaction, the type of the interaction (e. g. parasitic, pathogenic, mutualistic, or trophic interactions), the location (country) the interaction was reported from, and the publication source combined with detailed notes to each questionable entry comprised one record. Publications available in printed formats only were either digitized and data were extracted using semi-automatic text-mining processes, or they were manually screened. We aimed at possible completeness, using a wide range of databases and search engines and several languages to cover most of the published literature.

Both ground beetle and fungal names were validated and their higher taxonomical classifications were also extracted. When it was possible, historical localities were converted to their current country names. The full bibliographical details were also stored in the database.

The database covers a time-period from 1793 to 2020, spans over all geographic sub-regions defined by the United Nations (“UNSD — Methodology”, unstats.un.org. Retrieved 2020–10–11) with recorded associations from 129 countries. Our effort yielded 3,378 unique associations in 5,564 records between 1,776 carabid and 676 fungal species. Although rapidly developing molecular methods have largely facilitated the mapping of complex interaction networks in ecological studies^25,26,27, due to the historic nature of our dataset, most of the records rely on traditional taxonomical identification. Yet, 16 records were based purely on metabarcoding studies; comments linked to these associations clearly identify them.

Whilst we found relatively few pathogenic interactions, a great diversity between ectoparasitic Laboulbeniales fungi and carabids was revealed (Fig. 1). Soft bodied, cave-dwelling members of the Trechinae subfamily were particularly prone to these parasitic infections. Little information was available on mutualistic relationships but the presence of Yarrowia yeast reported from the gut of several carabid species²⁸ is probably beneficial for both parties. The data show two distinct peaks in publications registering new associations, in the early 19^th century and in the late 20^th century (Fig. 2a) but the steady increase in the cumulative number of associations (Fig. 2b) suggests that further research is required to fully resolve this association network. Although we believe that most of the data published so far were collected, data submission will remain open to researchers wishing to contribute.

Source: Ecology - nature.com