Lumbricid Earthworms Research Articles

Differential Influence of Soil Organic Carbon and Calcium on the Community of Lumbricid Earthworms as Ecosystem Engineers in Cool Temperate Forests of Hokkaido

Differential Influence of Soil Organic Carbon and Calcium on the Community of Lumbricid Earthworms as Ecosystem Engineers in Cool Temperate Forests of Hokkaido

Effect of Insecticide Exposure Across Multiple Generations of the Earthworm Eisenia andrei.

The toxicity of neonicotinoids and many of their replacement insecticides to nontarget soil invertebrates such as earthworms has previously been established. However, the long-term effects of these substances on these organisms are largely unknown. In the field of soil ecotoxicology, lumbricid earthworms such as Eisenia andrei are used extensively due to the availability of standardized test methods and their adaptability to laboratory culture and testing. Multigenerational studies have gained popularity and attention in recent years, with a shift toward the use of long-term assays and lower concentrations of test chemicals. The use of exposure concentrations that include those measured in a monitoring program carried out by the Government of Ontario presents a realistic exposure scenario that may not show significant effects in contemporary, shorter term studies. We used current standardized test methods as a basis for the development of multigenerational studies on E. andrei. The effects of exposure to a single application of the insecticides thiamethoxam and cyantraniliprole on the survival and reproduction of E. andrei were observed over three (thiamethoxam) or two (cyantraniliprole) generations using consecutive reproduction tests. No significant impacts on adult survival were reported in any generation for either insecticide, whereas reproduction decreased between the first and second generations in the thiamethoxam test, with median effective concentration (EC50) values of 0.022 mg/kg dry weight reported for the first generation compared with 0.002 mg/kg dry weight in the second generation. For cyantraniliprole, an EC50 of 0.064 was determined for the first generation compared with 0.016 mg/kg dry weight in the second generation. A third generation was completed for the thiamethoxam test, and a significant decrease in reproduction was observed in all treatments and controls compared with previous generations. No significant difference between thiamethoxam treatments and the control treatment was reported for the third generation. Collectively, these data indicate that exposure of oligochaetes to these two insecticides at concentrations representative of field conditions may result in long-term stresses. Environ Toxicol Chem 2024;43:2058-2070. © 2024 The Author(s). Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Earthworm co-invasion by Amynthas tokioensis and Amynthas agrestis affects soil microaggregate bacterial communities

Earthworms restructure the soil environment through burrowing, consumption, and casting behaviors. Though non-native European Lumbricid earthworms are well-studied in North American soils, the Asian pheretimoid Amynthas tokioensis and Amynthas agrestis earthworms exhibit distinct ecological patterns that alter invaded habitats. In particular, the combination of disruptive bioturbation with earthworm-driven aggregate formation may affect soil structure, C protection, and microbial community assembly processes, such as dispersal and selection. We aimed to determine the effects of A. tokioensis and A. agrestis co-invasions in woodlands in Madison, WI, U.S. on soil bacterial communities and edaphic characteristics. Using 16S rRNA gene sequencing, we found that the activity of these Amynthas species earthworms significantly affected bacterial community composition, however, sites demonstrated different responses in compositional dissimilarity (i.e., beta diversity), and the relative influences of homogenizing community assembly processes (i.e., homogeneous selection and homogenizing dispersal). Overall, inconclusive support for the hypothesized homogenization of bacterial community composition driven by homogenizing community assembly processes indicates that the effects of A. tokioensis and A. agrestis pressure in these systems represent a departure from previously established soil disturbance paradigms. Instead, we conclude that aggregate formation via A. tokioensis and A. agrestis casting activity does not consistently impose a strong selective filter on soil bacterial communities, nor does the heightened earthworm activity necessarily act to meaningfully homogenize soil communities via dispersal. Overall increases in soil C and N under A. tokioensis and A. agrestis activity support previous work indicating enhanced decomposition and incorporation of soil litter, but future work could focus on long-term fate of microaggregate-protected C.

The search finds an end: the morphologically chimeric hysterocinetids belong to the subclass Hymenostomatia (Ciliophora: Oligohymenophorea)

Abstract The digestive tract of oligochaetes harbours a diverse ciliate community embracing plagiotomids, nyctotherids, astomes, and hysterocinetids. Although several hundred intestinal ciliate species are known, only two hysterocinetids have been reported from the intestine of Holarctic lumbricid earthworms hitherto. The present study is focused on the taxonomy, morphology, and molecular phylogeny of two lumbricid-dwelling taxa, the insufficiently known Protoptychostomum simplex and Hysterocineta bellerophon sp. nov., detected in Central Europe. Diagnoses of the genera Protoptychostomum and Hysterocineta were improved taking into account also features of the oral ciliature for the first time. In the past, the proper classification of hysterocinetids in the class Oligohymenophorea was hampered by the dramatic remodelling of the anterior body end into a thigmotactic sucker, as well as by the helicalization and transfer of the oral apparatus to the posterior body pole. The present phylogenetic analyses of nuclear and mitochondrial genes robustly reject the classification of hysterocinetids in subclass Scuticociliatia or as a distinct subclass, Hysterocinetia. However, hysterocinetids were consistently and robustly nested deep in subclass Hymenostomatia in a sister-position to the free-living Tetrahymena paravorax. The hymenostome affinity of hysterocinetids is also corroborated by the parakinetal stomatogenesis and the stichodyad paroral membrane accompanied by three regularly organized membranelles.

APOLOCYSTIS BOSANQUETI N. SP. (APICOMPLEXA: EUGREGARINORIDA) FROM THE INVASIVE EARTHWORM AMYNTHAS AGRESTIS (ANNELIDA: MEGASCOLECIDAE), WITH SIGNIFICANCE FOR THE MONOPHYLY OF THE FAMILY MONOCYSTIDAE.

Apolocystis bosanqueti n. sp., a parasite of an important invasive earthworm in North America, Amynthas agrestis, is described from a site in northern Vermont. The earthworm host follows an annual life cycle in Vermont, so the entire life cycle of the parasite can be observed in 7 mo. In spring, the parasites were first seen in juvenile worms as paired gamonts (suggesting precocious association). These paired gamonts mature into gametocytes that form an opaque structure, with a thick gelatinous envelope (epicyst), that becomes full of zygotes. The resulting gametocyst becomes packed with ∼105 fusiform oocysts. The mature orbicular gametocysts are large (∼1 mm in diameter) and visible to the naked eye through the body wall of the host's anterior segments. The new species most resembles Apolocystis herculea described from many lumbricid earthworm species in Europe but differs from that parasite because Ap. herculea infects the intestinal wall in the posterior of the host rather than the anterior segments. A survey of 9 other earthworm species sympatric with Am. agrestis revealed that only Amynthas tokioensis, also an invasive species, was infected with Ap. bosanqueti, albeit much less commonly. Diagnosis for the family Monocystidae is problematic because cardinal characters are lacking, and the commonly cited character, a trophozoite with no anterior differentiation, is violated in most genera placed in the family. For the first time, a molecular phylogeny is presented that includes 3 genera of monocystids with diverse cell morphology (including the new species) and supports the monophyly of the family. The only morphological character that may be used to diagnose the Monocystidae is the morphology of oocysts, which are fusiform with extended terminal tips. A comparison of oocysts from 7 parasites recovered from local earthworms, including from 3 monocystid species in the phylogeny, confirms the utility of this diagnostic trait. The 2 hosts of the new species were most likely introduced from Japan, so the range of Apolocystis likely extends into East Asia.

Multidimensional stoichiometric mismatch explains differences in detritivore biomass across three forest types.

The ecological stoichiometry theory provides a framework to understand organism fitness and population dynamics based on stoichiometric mismatch between organisms and their resources. Recent studies have revealed that different soil animals occupy distinct multidimensional stoichiometric niches (MSNs), which likely determine their specific stoichiometric mismatches and population responses facing resource changes. The goals of the present study are to examine how long-term forest plantations affect multidimensional elemental contents of litter and detritivores and the population size of detritivores that occupy distinct MSNs. We evaluated the contents of 10 elements of two detritivore taxa (lumbricid earthworms and julid millipedes) and their litter resources, quantified their MSNs and the multidimensional stoichiometric mismatches, and examined how such mismatch patterns influence the density and total biomass of detritivores across three forest types spanning from natural forests (oak forest) to plantations (pine and larch forests). Sixty-year pine plantations changed the multidimensional elemental contents of litter, but did not influence the elemental contents of the two detritivore taxa. Earthworms and millipedes exhibited distinct patterns of MSNs and stoichiometric mismatches, but they both experienced severer stoichiometric mismatches in pine plantations than in oak forests and larch plantations. Such stoichiometric mismatches led to lower density and biomass of both earthworms and millipedes in pine plantations. In other words, under conditions of low litter quality and severe stoichiometric mismatches in pine plantations, detritivores maintained their body elemental contents but decreased their population biomass. Our study illustrates the success in using the multidimensional stoichiometric framework to understand the impact of forest plantations on animal population dynamics, which may serve as a useful tool in addressing ecosystem responses to global environmental changes.

Agroecology niche for New Zealand's native earthworms

Exotic lumbricid earthworms have had some limited success colonising productive agricultural pastures in New Zealand, in place of native megascolecid species that did not adapt to the conversion from native vegetation cover. Native earthworms in lowland intensively-farmed landscapes are now almost entirely restricted to small fragments of native vegetation on marginal land where they coexist with adventive lumbricids. In recent years, regular pasture replacement using cultivation has been largely replaced by herbicide spray-out followed by direct drilling; much less soil disturbance potentially creates a new opportunity for native earthworms to colonise pastures. Reclaiming native earthworm habitat is critical not only to protecting diversity, but also to sustaining New Zealand's unique soil ecosystem services strongly associated to role of native species; however, there have been no studies related to this. Using a mesocosm experiment, we investigated how native and exotic earthworms modify physicochemical properties of a sheep-grazed pasture soil. The pasture soil was found to be equally suitable for the growth and survival of native and exotic species. Most burrowing earthworms increased the more soluble forms of macronutrients (N, P, S, K and Mg), but differences between native and exotic species were found to be larger than between functional groups. Two species of native earthworms, Octochaetus multiporus and Maoridrilus transalpinus, modified some soil properties in similar way to exotic species, but had significantly different impacts on pH, mineralisation of nutrients, and plant availability of trace elements. Compared to control, plant available N (PAN) and S concentrations were higher by more than 100% and 40%, respectively, in soils with presence of burrowing activity of the two native earthworms. Future co-existence of communities of native and exotic earthworms in agricultural pastures appears realistic, and this would benefit conservation of native species as well as dairy production. Further research may also reveal additional and unique benefits to soil quality that could be attributable to this formerly unavailable niche for native earthworms.

Polymorphic microsatellite markers demonstrate hybridization and interspecific gene flow between lumbricid earthworm species, Eisenia andrei and E. fetida.

The lumbricid earthworms Eisenia andrei (Ea) and E. fetida (Ef) have been used as model organisms for studies on hybridization. Previously they have been identified by species specific sequences of the mitochondrial COI gene of maternal origin (‘a’ or ‘f’) and the nuclear 28S gene of maternal/paternal origin (‘A’ or ‘F’). In experimental crosses, these hermaphroditic species produce progeny of genotypes Ea (aAA), Ef (fFF) and hybrids (aAF and fFA) originating by self-fertilization or cross-fertilization. To facilitate studies on new aspects of the breeding biology and hybridization of earthworms, polymorphic microsatellite markers were developed based on 12 Ea and 12 Ef specimens and validated on DNA samples extracted from 24 genotyped specimens (aAA, fFF, aAF and fFA) from three laboratory-raised families and 10 of them were applied in the present study. The results indicate that microsatellite markers are valuable tools for tracking interspecific gene flow between these species.

Molecular data confirms the existence of distinct lineages within Lumbricus friendi (Cognetti 1904) and related “friends”

Lumbricus friendi is a lumbricid earthworm mainly found in western Europe, considerably less well studied than its close relative L. terrestris and until now, has not been a subject of taxonomical debate. However, its disjointed geographical distribution suggesting striking similarities to the Celtic fringes and of the so-called “Lusitanian” species merits further investigation. Our aim was to examine the genetic variation of this species and other related taxa within the genus (L. terrestris, L. rubellus, L. rubellus friendoides and L. friendi bouchei) to test for the existence of cryptic lineages that might explain its current distribution. Using mitochondrial (16S and COI) and nuclear (Amplified Fragment Length Polymorphism, AFLP) markers, we provide the first genetic basis not only to support the recent claim that L. friendi bouchei should be elevated to species rank (L. bouchei Zicsi and Csuzdi 1999), but also to conclude that L. rubellus friendoides is a valid species too, deserving a new name (L. heracleus stat. nov.). In addition, the AFLP results indicated the existence of a high cryptic diversity within L. friendi populations, which lacked geographic structure, resulting in the French samples being genetically closer to those from Ireland and Wales than to the Spanish ones. Our findings further highlight the likelihood that L. friendi and L. bouchei might have been overlooked or confounded with L. terrestris/L. herculeus and question the reliability of L. friendi records reported in the literature and those deposited in museums and sequence libraries (we provide evidence that this seem to be the case with two examples). We therefore advocate for a better link between morphological diagnostic characters and molecular sequences and the taxonomical validation of museums’ collections and sequence repositories.

Holistic evaluation of long-term earthworm field studies with a fungicide.

Plant protection products to be placed on the market in the European Union need to meet rigorous safety criteria including the testing of lumbricid earthworms, the functionally most important soil organism group in Central European agricultural ecosystems. To address uncertainties and investigate the potential long‐term in‐crop effects of the fungicide Cantus® containing 50% boscalid as an active substance, a series of standardized earthworm field studies with an overall duration of 5 years per study program was carried out in four German agricultural fields under realistic crop rotation conditions. A two‐step approach was chosen to analyze the potential overall long‐term effects on earthworms in agricultural fields: (i) an assessment of the earthworm abundance development in the course of the four study programs in relation to the determined actual content of boscalid in soil and (ii) an effect size meta‐analysis of earthworm abundance 1 year after treatment for each consecutive year and study program. Measured boscalid concentrations in the soil after multiple applications were well above the maximum boscalid residues observed in agricultural soils across Central Europe. There were isolated statistically significant reductions of earthworm abundance for some species and groups at some time points during the studies, but no consistent relationship to the Cantus® treatments was observed. These results were supported by the meta‐analysis, indicating no adverse effects on earthworm populations. Therefore, fluctuations of abundance reflect the natural variation of the populations rather than a concentration‐related response. Based on this comprehensive analysis, we conclude that there is no application rate‐related effect of the 5‐year use of Cantus® on the development of the earthworm communities. The four study programs, paired with a comprehensive evaluation, directly address the concerns about the potential long‐term effects of boscalid on earthworms in the field and suggest that multiyear applications do not adversely affect earthworm populations. Integr Environ Assess Manag 2022;18:1399–1413. © 2021 ECT Oekotoxikologie GmbH and BASF SE. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).

Diversity and Eco-Evolutionary Associations of Endosymbiotic Astome Ciliates With Their Lumbricid Earthworm Hosts.

Coevolution of endosymbionts with their hosts plays an important role in the processes of speciation and is among the most fascinating topics in evolutionary biology. Astome ciliates represent an interesting model for coevolutionary studies because they are so tightly associated with their host organisms that they completely lost the cell oral apparatus. In the present study, we used five nuclear markers (18S rRNA gene, ITS1–5.8S–ITS2 region, and 28S rRNA gene) and two mitochondrial genes (16S rRNA gene and cytochrome c oxidase subunit I) to explore the diversity of astomes inhabiting the digestive tract of lumbricid earthworms at temperate latitudes in Central Europe and to cast more light on their host specificity and coevolution events that shaped their diversification. The present coevolutionary and phylogenetic interaction-adjusted similarity analyses suggested that almost every host switch leads to speciation and firm association with the new host. Nevertheless, the suggested high structural host specificity of astomes needs to be tested with increased earthworm sampling, as only 52 out of 735 lumbricid earthworms (7.07%) were inhabited by ciliates. On the other hand, the diversification of astomes associated with megascolecid and glossoscolecid earthworms might have been driven by duplication events without host switching.

Multi-gene phylogeny of the subclass Astomatia (Protista: Ciliophora) refreshed with two rare astome ciliates from the digestive tube of endogeic earthworms

Astome ciliates are a diverse group of obligate endosymbionts, living in the alimentary tract of invertebrates and vertebrates. In the digestive tube of two endogeic lumbricid earthworms, we discovered Metaradiophrya speculorum sp. n. and re-discovered Maupasella mucronata after almost half a century. Their systematic positions were determined using the 18S rRNA gene, ITS1-5.8S-ITS2 region, and the barcoding D1/D2 domains of the 28S rRNA gene. According to the present phylogenetic analyses, astomes isolated from the alimentary tract of endogeic earthworms form a diverse paraphyletic assemblage, whose crown radiation contains species isolated from anecic and epigeic earthworms. The genus Metaradiophrya was depicted as monophyletic in multi-gene analyses and its taxa clustered according to the ecological groups of their host earthworms. The traditional classifications of the genus Metaradiophrya within the family Radiophryidae, which is characterized by a Λ-shaped attachment organelle, was however questioned. Genetic data suggested Metaradiophrya to be closely related to Anoplophrya, which does not possess any holdfast organelles and belongs to the family Anoplophryidae. The genus Maupasella was traditionally classified in the nominotypical family Maupasellidae, which is defined by the presence of a short, apical attachment spine. Interestingly, genetic data suggested that Maupasella represents an “orphan” lineage within the endogeic cluster, with some affinity to Subanoplophrya, which lacks holdfast organelles. Since there is only little correlation between the morphology-based and molecular classifications of astomes, the reconciliation of both frameworks will require accounting for adaptive radiation and host-driven diversification—two phenomena that have very likely shaped the evolution of astomes.

Tools for monitoring and study of peregrine pheretimoid earthworms (Megascolecidae)

Peregrine pheretimoid earthworms, commonly known as jumping worms, are members of the family Megascolecidae that have become widely established outside of their native ranges. In many parts of the world this represents a second wave of earthworm invasions, following the introduction of peregrine European earthworms in the family Lumbricidae during the colonial era. Forest ecologists, turf managers, gardeners, and other land managers are concerned about the observed or presumed negative effects of jumping worms on invaded habitats. Although research on jumping worms has accelerated in recent decades, our understanding of their ecology remains limited. We compiled techniques useful to researchers working to fill voids in our understanding. Similar past efforts have focused on tools used to study common European species. Differences in life cycle, behavior, morphology, and physiology make it difficult to transfer experiences with European earthworms to pheretimoids. For example, the loss of reproductive features in many pheretimoid populations poses a challenge for identification, and techniques for individually tagging lumbricid earthworms have been less successful for megascolecids. The active and ongoing expansion of pheretimoid populations in many areas requires increased attention on distributed methods, such as citizen-science protocols, for detecting and tracking their expansion. Finally, the desire to limit populations of pheretimoids, including those invading gardens and other environments that might be successfully restored, has exposed the lack of options for targeted, effective control of unwanted earthworms. We identify opportunities to address these voids in our methodological tool kit and encourage the adaptation of techniques previously used in the study and management of other invasive animals.

Impairment of reproductive capabilities in three subsequent generations of asymmetric hybrids between Eisenia andrei and E. fetida from French, Hungarian and Polish laboratory colonies.

Eisenia andrei (Ea) and E. fetida (Ef) lumbricid earthworms are simultaneous hermaphrodites potentially capable of self-fertilization and hybridization. We have shown previously that reproductive isolation in these species is incomplete in Ea and Ef earthworms of French provenance, as viable offspring appeared in inter-specific pairs. Fertile asymmetric hybrids developed from Ea-derived ova fertilized by Ef-derived spermatozoa, as well as Ea or Ef specimens derived after self-fertilization (resulting from admixture of endogenously produced spermatozoa with sperm from a partner), but never Ef-hybrids from Ef-ova fertilized by Ea-spermatozoa. The latter appeared only in backcrosses of Ea-hybrids with the Ef. Here we show that these phenomena are not unique for French Ea/Ef earthworms, but are shared by earthworms from French, Hungarian, and Polish laboratory cultures. Semi-quantitative studies on fertility of Ea-derived hybrids revealed gradually decreasing numbers of offspring in three successive generations, more rapid in backcrosses with Ef than with Ea, and the absence of progeny in pairs of hybrids, despite the presence of cocoons in almost all pairs. Based on species specific mitochondrial and nuclear DNA sequences, we provide the first examples of two unique sterile hybrids with mitonuclear mismatch and potential mitonuclear incompatibility among offspring of one of the hybrid+Ef pairs. Earthworms from the investigated populations did not reproduce when kept from hatching in isolation or with representatives of Dendrobaena veneta but started reproducing upon recognition of a related partner, such as Ea, Ef or their hybrids. The existence of Ea or Ef specimens among offspring of hybrid+Ea/Ef pairs might be explained either by partner-induced self-fertilization of Ea/Ef or hybrid-derived ova, or by cross-fertilization of Ea/Ef /hybrid ova by partner-derived spermatozoa; the latter might contribute to interspecific gene introgression.

Annual Reproductive Performance of Eisenia andrei and E. fetida 2 in Intra- and Inter-Specific Pairs and Lack of Reproduction of Isolated Virgin Earthworms

Eisenia andrei/fetida complex of lumbricid earthworms contains E. andrei (Ea) and two mitochondrial lineages of E. fetida (Ef), referred to as Ef1 and Ef2. These earthworms are hermaphrodites capable of self-fertilization and hybridization as evidenced in laboratory mated earthworms from Ea and Ef1 lineage of Ef. The aim of the present investigations was to compare reproductive performance of Ea and Ef2 lineage from French laboratory stocks reared for a decade in Polish laboratories. These were cultured either in isolation and/or in intra-specific or inter-specific pairs for up to 57 weeks from hatching. Parental specimens and offspring were identified by species/lineage-specific sequences of the haploid mitochondrial COI gene, either 'a' or 'f2', and species-specific sequences of the nuclear 28s rRNA gene, either 'AA' or 'FF', thus delimitated as aAA or f2FF for Ea or Ef2, respectively, or aAF for hybrids. Isolated virgin earthworms produced a few sterile cocoons only, more frequently in Ef2 than in Ea, but no hatchlings. Analysis of cocoon production and reproduction of laboratory-mated intra-specific Ea+Ea and Ef2+Ef2 pairs revealed higher fecundity of Ea than Ef2 measured by numbers of cocoons and hatchlings, while inter-specific Ea+Ef2 pairs gave plenty cocoons but low numbers of aAF hybrids developed from Ea ova fertilized by Ef2 spermatozoa.

Delimitation of five astome ciliate species isolated from the digestive tube of three ecologically different groups of lumbricid earthworms, using the internal transcribed spacer region and the hypervariable D1/D2 region of the 28S rRNA gene

BackgroundVarious ecological groups of earthworms very likely constitute sharply isolated niches that might permit speciation of their symbiotic ciliates, even though no distinct morphological features appear to be recognizable among ciliates originating from different host groups. The nuclear highly variable ITS1–5.8S-ITS2 region and the hypervariable D1/D2 region of the 28S rRNA gene have proven to be useful tools for the delimitation of species boundaries in closely related free-living ciliate taxa. In the present study, the power of these molecular markers as well as of the secondary structure of the ITS2 molecule were tested for the first time in order to discriminate the species of endosymbiotic ciliates that were isolated from the gastrointestinal tract of three ecologically different groups of lumbricid earthworms.ResultsNineteen new ITS1–5.8S-ITS2 region and D1/D2-28S rRNA gene sequences were obtained from five astome species (Anoplophrya lumbrici, A. vulgaris, Metaradiophrya lumbrici, M. varians, and Subanoplophrya nodulata comb. n.), which were living in the digestive tube of three ecological groups of earthworms. Phylogenetic analyses of the rRNA locus and secondary structure analyses of the ITS2 molecule robustly resolved their phylogenetic relationships and supported the distinctness of all five species, although previous multivariate morphometric analyses were not able to separate congeners in the genera Anoplophrya and Metaradiophrya. The occurrence of all five taxa, as delimited by molecular analyses, was perfectly correlated with the ecological groups of their host earthworms.ConclusionsThe present study indicates that morphology-based taxonomy of astome ciliates needs to be tested in the light of molecular and ecological data as well. The use of morphological identification alone is likely to miss species that are well delimited based on molecular markers and ecological traits and can lead to the underestimation of diversity and overestimation of host range. An integrative approach along with distinctly increased taxon sampling would be helpful to assess the consistency of the eco-evolutionary trend in astome ciliates.

Invasive lumbricid earthworms in North America - different life-histories but common dispersal?

Lumbricid earthworms are invasive across northern North America, causing notable changes in forest ecosystems. During their range expansion they encountered harsher climatic conditions compared to their native ranges in evolutionary short time. This study investigated if (1) dispersal barriers, (2) climatic selection, or (3) anthropogenic activities, such as fishing bait disposal, structure the dispersal of free-living earthworm populations. North America, forest habitats along former Wisconsinan glaciation line. Lumbricus terrestris, L. rubellus. Lumbricus terrestris and L. rubellus co-occur in the same habitats but differ in ecology and use Conservation approach for goblin species were sampled in five transects ranging from the east to the west coast of northern North America, including major dispersal barriers, three different climate zones, and bait shops near sampling locations. Genetic diversity and structure were compared between the two species, and the presence of free-living bait shop genotypes was assessed using four markers (COI, 16S rDNA, 12S rDNA, H3). Populations of both species were genetically diverse with some geographic structure, which was more pronounced in L. terrestris than in L. rubellus. Common haplotypes were present in all regions, but locally restricted haplotypes also occurred. Further, two distinct genetic clades of L. terrestris co-occurred only in the two most distant transects (Alberta and Minnesota). Genotypes identical to bait individuals were omnipresent in field populations of L. terrestris. Genetic diversity was high in both species, and invasive populations represented a genetic subset of European earthworms. Geographic and climatic dispersal barriers affected the less mobile species, L. rubellus, resulting in differences in genetic structure between the two species. Our results indicate common long-distance dispersal vectors and specific vectors affecting only L. terrestris. The roles of climate and anthropogenic activities are discussed, providing additional explanations of dispersal and new insights into establishment of invasive earthworms.

Niche-structured assemblages of exotic earthworms in headwater streambanks in eastern New York State, USA

In eastern North America, most Lumbricid earthworms found today above the post-Wisconsin Glacial boundary are non-indigenous, some with marked potential as invasive and ecologically disruptive species. These earthworms tend to appear as assemblages, not solitary species. Among potential explanations are successional facilitation among taxa, anthropogenic dispersal mechanisms that promote multi-species introductions, or simply shared habitat determinants that lead to accumulations through various dispersal pathways. We examined headwater streambanks in higher elevation forests of eastern New York State, and found up to 15 lumbricid earthworm species per 50 m-long reach among 14 sites divided between two montane regions, the northern Catskill Mountains and the Helderberg Plateau of eastern New York State.After pooling six surveys per site taken over two years, we found consistent differences between the two regions. Although most species (14/18) were found in both regions, their relative abundances and assortment patterns differed. Eisenoides lonnbergi and Bimastos rubidus, two native species were more prevalent in the Catskills, and represented new records for both regions. Ordination (CCA) on a set of measured environmental parameters revealed that most species were distributed along a soil pH-tree composition gradient. At the site level, clustering was strongly regional, despite a relatively small distance (<25 km) separating the regions. In all, several determinants may be at work in shaping observed earthworm assemblages. However, we did not detect evidence for interspecific interactions as a structuring element. When tested with a null model simulation, observed pairwise species associations did not depart significantly from random expectations (z-tests, p > 0.30 for both regions). Furthermore, the riparian zones we surveyed are relatively dynamic settings, so the stability of these novel assemblages is uncertain. With other invasive earthworm species now spreading throughout New York State, that uncertainty may grow.

Invasive lumbricid earthworms in northeastern North American forests and consequences for leaf-litter fauna

Colonization of North America by exotic earthworms has been implicated in undesirable changes in soil structure, nutrient cycling, and biodiversity. Invasion by putative European earthworms has a long history in northeastern North America. Partly for this reason, factors that may be continuing to facilitate expansion of earthworm distributions and the consequences of earthworm spread in the Northeast get relatively little attention. We sampled earthworms and environmental attributes at 85 sites in central New York. We additionally sampled leaf-litter fauna at 25 of these sites. We detected no earthworms at 27 of 71 forested sites (38%). Forested sites without detectable earthworm populations were farther from the nearest road and had soils of lower pH than forested sites with earthworms. Proximity of the nearest road was strongly associated with earthworm diversity and abundance, and earthworm biomass was highest in low, moist areas. We found a strong, negative relationship between the biomass of earthworms and abundance of invertebrates in the litter layer. This association was likely mediated by the abundance of organic litter, which was lower at sites with high biomass of earthworms. Sites with only the putative native Bimastos (Dendrodrilus) rubidus had a high mass of leaf litter and large numbers of leaf litter animals despite high densities of this species. We believe that there is potential for further expansion of European earthworm taxa in the Northeast and strong evidence for negative consequences of this expansion. Additional regulations on activities that promote introduction may be necessary.

Assessing the Impact of Lumbricid Earthworms on Forest Seeds in Northeastern Ohio

This study examines the capacity of two nonnative lumbricid earthworms, Lumbricus terrestris and L. rubellus, to ingest and digest the seeds of herbaceous plants and affect their distribution in forest soils of northeastern Ohio. A survey of earthworms in a forested area of Cleveland Metroparks revealed Lumbricus was the most common and widely distributed earthworm genus, although Aporrectodea and Octolasion were also well represented. A total of 120 soil samples taken adjacent to earthworm sampling plots and placed in a growth chamber yielded a total of 35 germinations. The germinations occurred primarily in the upper 8 cm of the soil profile, suggesting limited redistribution of seeds by earthworms. Growth chamber feeding trials using seeds ranging in size from approximately 2 to 5 mm maximum linear dimension revealed that both species of earthworm will consume and digest seeds that measure up to between 3 and 4 mm. Lumbricus terrestris consistently ingested and digested more than twice as many seeds as did the substantially smaller L. rubellus. Comparisons of the germination rates of seeds egested by the earthworms with rates for seeds that were not ingested showed no impact on germination due to egestion, suggesting ingestion and subsequent egestion of seeds by lumbricid earthworms does not enhance germination. By ingesting and digesting seeds, L. rubellus and L. terrestris should reduce the number of viable seeds in the soil and, thereby, contribute to changes in forest vegetation.