Dietary flexibility aids Asian earthworm invasion in North American forests

Abstract

On a local scale, invasiveness of introduced species and invasibility of habitats together determine invasion success. A key issue in invasion ecology has been how to quantify the contribution of species invasiveness and habitat invasibility separately. Conventional approaches, such as comparing the differences in traits and/or impacts of species between native and/or invaded ranges, do not determine the extent to which the performance of invaders is due to either the effects of species traits or habitat characteristics. Here we explore the interaction between two of the most widespread earthworm invaders in the world (Asian Amynthas agrestis and European Lumbricus rubellus) and study the effects of species invasiveness and habitat invasibility separately through an alternative approach of "third habitat" in Tennessee, USA. We propose that feeding behaviors of earthworms will be critical to invasion success because trophic ecology of invasive animals plays a key role in the invasion process. We found that (1) the biomass and isotopic abundances (delta13C and delta15N) of A. agrestis were not impacted by either direct effects of L. rubellus competition or indirect effects of L. rubellus-preconditioned habitat; (2) A. agrestis disrupted the relationship between L. rubellus and soil microorganisms and consequently hindered litter consumption by L. rubellus; and (3) compared to L. rubellus, A. agrestis shifted its diet more readily to consume more litter, more soil gram-positive (G+) bacteria (which may be important for litter digestion), and more non-microbial soil fauna when soil microorganisms were depleted. In conclusion, A. agrestis showed strong invasiveness through its dietary flexibility through diet shifting and superior feeding behavior and its indirectly negative effect of habitat invasibility on L. rubellus via changes in the soil microorganism community. In such context, our results expand on the resource fluctuation hypothesis and support the superior competitor hypothesis. This work presents additional approaches in invasion ecology, provides some new dimensions for further research, and contributes to a greater understanding of the importance of interactions between multiple invading species.

Earthworms facilitate carbon sequestration through unequal amplification of carbon stabilization compared with mineralization

“…Soil (0-5 cm) and earthworms were collected from a B2 km 2 area on the western edge of the Great Smoky Mountains National Park (35°31 0 30 00 -35°33 0 27 00 N; 83°59 0 35 00 -84°00 0 36 00 W). Detailed descriptions of soil and vegetation at the field site are provided elsewhere 22 . Nine samples of field soil were collected and freezedried for measurements of stable isotope ratios (d 15 N and d 13 C) and SOC content.…”

“…where f b is the earthworm background carbon fraction, which was assumed to be 0.75 as the experimental duration was short 22 , D represents the enrichment factor of earthworms from their putative diets, which was assumed to be 3.68% (ref. 22), f litter' and f soc' are fractions of litter and SOC-derived carbon, respectively, in earthworm biomass at the end of the 31 day incubation; d 13 C worm À t0 and d 13 C worm À t1 represent 13 C abundance of earthworms at the zero time and 31 days later, respectively; d 13 C litter and d 13 C soc are the same as in equation 3.…”

“…22), f litter' and f soc' are fractions of litter and SOC-derived carbon, respectively, in earthworm biomass at the end of the 31 day incubation; d 13 C worm À t0 and d 13 C worm À t1 represent 13 C abundance of earthworms at the zero time and 31 days later, respectively; d 13 C litter and d 13 C soc are the same as in equation 3. The total litter and SOC-derived carbon in earthworm tissues were then calculated with the combination of data such as earthworm biomass, water content (assumed to be 0.75) and earthworm carbon content.…”

“…The comparatively soilpreferring Asian Amynthas agrestis and litter-preferring European Lumbricus rubellus are used to establish distinct interactive systems of earthworm and microbiota 22 . Our data reveal that earthworms accelerate soil C mineralization, but do not increase the total amount of C mineralized compared with soil microbiota alone; in contrast, earthworm presence significantly enhances soil C stabilization.…”

Asian pheretimoid earthworms in North America north of Mexico: An illustrated key to the genera Amynthas, Metaphire, Pithemera, and Polypheretima (Clitellata: Megascolecidae)

“…Competition for leaf litter has been demonstrated between M. hilgendorfi and Lumbricus rubellus, one of the most common European earthworm species, with M. hilgendorfi being the superior competitor (Chang et al 2016a). Lumbricus rubellus also suffered reduced biomass in the presence of A. agrestis (Zhang et al 2010). Although invasion by these pheterimoids is often visible and dramatic, the consequences to ecosystem function remain unclear.…”