First field estimation of greenhouse gas release from European soil-dwelling Scarabaeidae larvae targeting the genus Melolontha

Abstract

Arthropods are a major soil fauna group, and have the potential to substantially influence the spatial and temporal variability of soil greenhouse gas (GHG) sinks and sources. The overall effect of soil-inhabiting arthropods on soil GHG fluxes still remains poorly quantified since the majority of the available data comes from laboratory experiments, is often controversial, and has been limited to a few species. The main objective of this study was to provide first insights into field-level carbon dioxide (CO 2 ), methane (CH 4 ), and nitrous oxide (N 2 O) release of soil-inhabiting larvae of the Scarabaeidae family. Larvae of the genus Melolontha were excavated at various sites in west-central and southern Germany, covering a wide range of different larval developmental stages, larval activity levels, and vegetation types. Excavated larvae were immediately incubated in the field to measure their GHG production. Gaseous carbon release of individual larvae showed a large inter- and intra-site variability which was strongly correlated to larval biomass. This correlation persisted when upscaling individual CO 2 and CH 4 production to the plot scale. Field release estimates for Melolontha spp. were subsequently upscaled to the European level to derive the first regional GHG release estimates for members of the Scarabaeidae family. Estimates ranged between 10.42 and 409.53 kt CO 2 yr -1 , and 0.01 and 1.36 kt CH 4 yr -1 . Larval N 2 O release was only sporadically observed and not upscaled. For one site, a comparison of field- and laboratory-based GHG production measurements was conducted to assess potential biases introduced by transferring Scarabaeidae larvae to artificial environments. Release strength and variability of captive larvae decreased significantly within two weeks and the correlation between larval biomass and gaseous carbon production disappeared, highlighting the importance of field measurements. Overall, our data show that Scarabaeidae larvae can be significant soil GHG sources and should not be neglected in soil GHG flux research.

Larvae of an invasive scarab increase greenhouse gas emissions from soils and recruit gut mycobiota involved in C and N transformations

“…CH 4 emission rates from isolated JB larvae in our study (1.0 ± 0.1 μg CH 4 h −1 larva −1 ) was similar to that observed in other isolated scarab larvae ( Bayon, 1980 ; Hackstein and Stumm, 1994 ; Cazemier et al, 2003 ; Lemke et al, 2003 ; Hackstein and van Alen, 2018 ; Brune, 2019 ; Görres and Kammann, 2020 ). In these insects, CH 4 production occurs in the enlarged hindgut compartment ( Bayon, 1980 ; Lemke et al, 2003 ) as a product of anaerobic respiration by methanogen prokaryotes that are part of the JB gut microbiota ( Chouaia et al, 2019 ; Avila-Arias et al, 2022 ).…”

“…As previously observed in other soil-dwelling scarab larvae ( Majeed et al, 2014 ; Görres and Kammann, 2020 ) and various soil fauna ( Kuiper et al, 2013 ; Lubbers et al, 2013 ; Filser et al, 2016 ; Soper et al, 2019 ), our results demonstrate that JB larvae both directly and indirectly affect soil GHG emission. Direct gas emissions results from physiological processes such as larval respiration and metabolism.…”

“…Invasive scarab beetles are among the many soil organisms that contribute to processes resulting in the production of soil greenhouse gases (GHGs; Hackstein and Stumm, 1994 ; Majeed et al, 2014 ; Hackstein and van Alen, 2018 ; Görres and Kammann, 2020 ). However, its invasiveness and status as a serious agricultural pest make the Japanese beetle Popillia japonica Newman (JB) unique with respect to its potential global impacts.…”

“…Although underrepresented in the literature, soil fauna may influence GHG fluxes directly via metabolism and respiration, and indirectly by influencing plant productivity and soil processes through a combination of activities. These activities include herbivory, dispersion of or grazing on microorganisms, fragmentation and redistribution of organic matter, defecation of microbes and nutrient rich compounds, and soil aggregate formation ( Kuiper et al, 2013 ; Lubbers et al, 2013 ; Filser et al, 2016 ; Gan et al, 2018 ; Gan and Wickings, 2020 ; Görres and Kammann, 2020 ). Although their importance and abundance in soil is undisputed, the magnitude of the effect of soil fauna on net soil GHG emissions remains poorly quantified with investigations limited to only a few species.…”

“…Arthropods comprise the vast majority of soil macrofauna (97%; Decaëns et al, 2006 ) and several taxa, including millipedes, cockroaches, termites, and scarab beetles, have been associated with increased GHG emissions from the soil ( Hackstein and Stumm, 1994 ; Hackstein and van Alen, 2018 ). Aside from their negative impacts on the productivity and sustainability of managed ecosystems, scarab beetles produce all three major GHGs (CO 2 , CH 4 , and N 2 O; Majeed et al, 2014 ; Görres and Kammann, 2020 ) with an estimated contribution of 0.2%–1.8% of total soil N 2 O emissions in tropical areas of the planet. In light of their contribution to GHG emissions from soil, their growing importance as agricultural pests, and growing global distribution as a consequence of climate change ( Kistner-Thomas, 2019 ), the larvae of invasive, soil-dwelling scarabs represent an understudied, but potentially important driver of global GHG emissions presently and in the future.…”