Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon

Abstract

a b s t r a c tSoil respiration is frequently measured as a surrogate for biological activities and is important in soil carbon cycling. The heterotrophic component of soil respiration is primarily driven by microbial decomposition of leaf litter and soil organic matter, and is partially controlled by resource availability. In North American temperate deciduous forests, invasive European and Asian earthworms are known to variously affect soil properties and resource availability through their feeding, burrowing, and casting behaviors, and may affect different components of soil respiration through modulating the microbial communities. By tracing litter-derived C from 13 C and 15 N double-enriched leaf litter into soil and CO 2 efflux in a mesocosm experiment, we tested the hypothesis that earthworms inhibit litter C-derived soil respiration by reducing resource availability and microbial biomass, and further examined how speciesspecific effects of earthworms on soil respiration are mediated by soil microbial community. We showed that while earthworms generally had no effect on total soil respiration, the interaction between Octolasion lacteum and Lumbricus rubellus had a significant negative non-additive effect, presumably through affecting anaerobic microsites in the soil. Moreover, litter C-derived soil respiration was reduced by the Asian Amynthas hilgendorfi, the European L. rubellus, and the North American native species Eisenoides lonnbergi, but not by the European species O. lacteum. Phospholipid fatty acid (PLFA) analysis and structural equation modeling indicated that while soil bacteria and fungi abundances were affected by earthworm species identities, the observed reduction of litter C-derived soil respiration could not be fully explained by changes in microbial biomass. We attributed these effects to earthworm-induced aggregate formation, reduction of microbial transformation of labile carbon, and antimicrobial peptide activities, and concluded that the mechanisms through which the four earthworm species affect the fate of litterderived C and its mineralization are species-specific.

Earthworms Building Up Soil Microbiota, a Review

“…In mesocosms with soil from arable fields (3.8% of organic matter) and potato residues on the surface, the endogeic Aporrectodea caliginosa did not impact soil microbial biomass which was obtained from the biovolume of bacterial numbers measured by confocal laser scanning microscopy (Postma-Blaauw et al, 2006). In contrast, Chang et al (2016) found an increase in the bacterial biomass of a forest soil mixed with litter, measured through PLFA, in the presence of Octolasion lacteum. Similar findings were reported for a pot experiment by Braga et al (2016), who detected increases in the bacterial 16S rRNA gene abundance in soils with the tropical earthworm Pontoscolex corethrurus, compared with soils without earthworms.…”

Forest and Rangeland Soil Biodiversity

“…However, reported results from case studies describing impacts on microbial biomass in the overall soil profile have ranged from positive (Groffman et al 2004(Groffman et al , 2015, to neutral (Snyder et al 2011), to negative (Eisenhauer et al 2007). Some of the observed differences can likely be attributed to earthworm species identities and interspecific interactions (Chang et al 2016). By changing the soil structure, soil organic matter properties, and soil microbial community, invasive earthworms may change C use efficiency of soil microbes, increase soil microbial biomass carrying capacity, and promote C metabolism (Dempsey et al 2013;Groffman et al 2015).…”

Biocontrol of invasive pheretimoid earthworms using Beauveria bassiana

“…Although there are several native North American earthworms’ species in northern North America ( McCay et al, 2017 ), most invasive species were introduced from Europe ( Gates, 1982 ) and Asia ( Kinberg, 1867 ). A second wave of invasions by Asian earthworms, collectively named “pheretimoids”, is currently in progress in North America ( Chang, Szlavecz & Buyer, 2016 ). The monetary cost of earthworm invasions has not been quantified probably because of the cryptic nature of the invasion and the “social standing” of earthworms.…”

“…Pheretimoids have become a leading ecological concern in hardwood forests in the northern USA ( Reynolds, 2015 ; Görres & Melnichuk, 2012 ; Migge-Kleian et al, 2006 ). Of the 16 pheretimoid species known to be present in North America ( Chang, Szlavecz & Buyer, 2016 ), three frequently co-invade in North America: Amynthas agrestis , A. tokioensis and Metaphire hilgendorfi ( Chang et al, 2018 ). The northerly expansion ( Moore, Görres & Reynolds, 2018 ; Görres et al, 2018 ) of the three co-invading pheretimoid species may be due to the lengthening of the growing season in the past 30 years ( Hayhoe et al, 2007 ; Bohlen et al, 2004 ).…”