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Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees.

ABSTRACT: Recent research shows that earthworms can alter defense traits of plants against herbivores and pathogens by affecting soil biochemistry. Yet, the effects of invasive earthworms on defense traits of native plants from previously earthworm-free ecosystems as well as the consequences for multitrophic interactions are virtually unknown.Here we use a combination of an observational study and a complementary experimental study to investigate the effects of invasive earthworms on leaf defense traits, herbivore damage and pathogen infection in two poplar tree species (Populus balsamifera and Populus tremuloides) native to North American boreal forests.Our observational study showed that earthworm invasion was associated with enhanced leaf herbivory (by leaf-chewing insects) in saplings of both tree species. However, we only detected significant shifts in the concentration of chemical defense compounds in response to earthworm invasion for P. balsamifera. Specifically, leaf phenolic concentrations, including salicinoids and catechin, were lower in P. balsamifera from earthworm-invaded sites.Our experimental study confirmed an earthworm-induced reduction in leaf defense levels in P. balsamifera for one of the defense compounds, tremulacin. The experimental study additionally showed that invasive earthworms reduced leaf dry matter content, potentially increasing leaf palatability, and enhanced susceptibility of trees to infection by a fungal pathogen, but not to aphid infestation, in the same tree species. Synthesis. Our results show that invasive earthworms can decrease the concentrations of some chemical defense compounds in P. balsamifera, which could make them susceptible to leaf-chewing insects. Such potential impacts of invasive earthworms are likely to have implications for tree survival and competition, native tree biodiversity and ecosystem functioning.

SUBMITTER: Thakur MP

PROVIDER: S-EPMC7891629 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees.

Thakur Madhav P MP Künne Tom T Unsicker Sybille B SB Biere Arjen A Ferlian Olga O Pruschitzki Ulrich U Thouvenot Lise L Türke Manfred M Eisenhauer Nico N

The Journal of ecology 20201009 2

Recent research shows that earthworms can alter defense traits of plants against herbivores and pathogens by affecting soil biochemistry. Yet, the effects of invasive earthworms on defense traits of native plants from previously earthworm-free ecosystems as well as the consequences for multitrophic interactions are virtually unknown.Here we use a combination of an observational study and a complementary experimental study to investigate the effects of invasive earthworms on leaf defense traits, ...[more]

PMID: 33664527

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Project description:Asian pheretimoid earthworms (e.g. Amynthas and Metaphire spp.) are invading North American forests and consuming the vital detrital layer that forest floor biota [including the keystone species Plethodon cinereus (Eastern Red-backed Salamander)], rely on for protection, food, and habitat. Plethodon cinereus population declines have been associated with leaf litter loss following the invasion of several exotic earthworm species, but there have been few studies on the specific interactions between pheretimoid earthworms and P. cinereus. Since some species of large and active pheretimoids spatially overlap with salamanders beneath natural cover objects and in detritus, they may distinctively compound the negative consequences of earthworm-mediated resource degradation by physically disturbing important salamander activities (foraging, mating, and egg brooding). We predicted that earthworms would exclude salamanders from high quality microhabitat, reduce foraging efficiency, and negatively affect salamander fitness. In laboratory trials, salamanders used lower quality microhabitat and consumed fewer flies in the presence of earthworms. In a natural field experiment, conducted on salamander populations from "non-invaded" and "pheretimoid invaded" sites in Ohio, salamanders and earthworms shared cover objects ~60% less than expected. Earthworm abundance was negatively associated with juvenile and male salamander abundance, but had no relationship with female salamander abundance. There was no effect of pheretimoid invasion on salamander body condition. Juvenile and non-resident male salamanders do not hold stable territories centered beneath cover objects such as rocks or logs, which results in reduced access to prey, greater risk of desiccation, and dispersal pressure. Habitat degradation and physical exclusion of salamanders from cover objects may hinder juvenile and male salamander performance, ultimately reducing recruitment and salamander abundance following Asian earthworm invasion.

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Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees.

Publications

Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees.

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