Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

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Lumbricus rubellus

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Lumbricus rubellus

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Identity

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Preferred Scientific Name

  • Lumbricus rubellus

International Common Names

  • English: leaf worm

Summary of Invasiveness

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The earthworm L. rubellus is thought to be native to Western Europe, but is now globally distributed in temperate and mild boreal climates. It is invasive species even within parts of Europe that have indigenous earthworms of similar ecology. Most invasions can be attributed to human activity, such as the movement of plants and soils, and, importantly, the transport of L. rubellus as fish bait (Tomlin, 1983; Hale et al., 2005a,b). The change in the soil structure, microbial community content and chemistry of the forest floor caused by introduced L. rubellus can be profound (Eisenhauer et al., 2007) and is likely to affect soil invertebrates. Plant communities are also affected (Holdsworth et al., 2007a,b), with reduced diversity of the forest floor herb layer and the promotion of some invasive plants. Little is known about the properties which make L. rubellus so invasive.

A good compilation of invasive earthworms can be found in Blakemore (2006).

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Annelida
  •             Class: Oligochaeta
  •                 Order: Haplotaxida
  •                     Family: Lumbricidae
  •                         Genus: Lumbricus
  •                             Species: Lumbricus rubellus

Notes on Taxonomy and Nomenclature

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In DNA barcodes (Hebert et al., 2003) of L. rubellus there are two distinct lineages, but there has been no attempt to investigate morphological variation in relation to these lineages. DNA barcoding is quite effective on earthworms (Richard et al., 2009). It is not yet clear if the two lineages represent distinct species, or if there are more lineages yet to be discovered.

There are 11 species and subspecies names in the synonymy of L. rubellus. Barcode-identified genetic lineages could match some of these taxa, but determining this will require extensive resampling of type localities and examination of type material. However, the type locality of the species is unknown, and there are no type specimens. With advanced DNA sequencing technologies it might be possible to obtain usable information from the degraded DNA of formaldehyde-treated specimens. This would then allow type material to be compared with lineages detected in modern populations.

Description

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External Features

Length 60-130 mm, diameter 3-4 mm, segment number 100-120. Body cylindrical in cross section except for slightly flattened posterior. Head end purplish red-dorsally, dorsal pigmentation fading towards posterior. Prostomium tanylobous (bearing two small furrows on the dorsal side the first segment, each furrow reaching the first intersegmental boundary), dorsal pores from furrow 7/8; spermathecal pores lateral in furrows 9/10/11 near level of setae C. Male pores in small slits in 15, clitellum 27-32, tubercular ridge 28-31. Setae are closely paired, the ventral setae (A) more widely spaced than the ventral couple (A and B), the distance between B and C close to the AA distance, and the CD distance slightly less than AB. Small papillae surround setae A and B on segments of the clitellum.

Internal Features

Septa present from 4/5; 7/8/9 strongly muscularized. Gizzard in 17, typhlosole begins in 21. Last pair of hearts in 11. Seminal vesicles in 9, 11 and 12; spermathecae in 9 and 10.

Sims and Gerard (1999), Schwert (1990), Reynolds (1977) and Blakemore (2006) contain keys with L. rubellus.

Juveniles are not reliably identifiable by any means other than molecular data, for which the DNA barcode region is recommended.  Egg capsules cannot be reliably identified without molecular tools.

Distribution

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L. rubellus is believed to have originated in Western Europe. As Gates (1972) commented, determining the native range of the common invasive earthworms of Europe could be impossible after over 2000 years of human-mediated transportation. At present, the task could be possible with the use of molecular techniques, but it would require extensive sampling of populations in western and central Europe. The genus Lumbricus could have a native range from the Pyrenees, across France and through Austria, parts of southern Germany, Hungary and Romania.

Pleistocene glaciations are thought to have eliminated the earthworm fauna from most northern temperate regions worlwide (Tiunov et al., 2006). Natural repopulation by dispersal from southern glacial refugia in North America, Europe and Asia has been slow (e.g. ~10 m y-1; Terhuivo and Saura, 2006), leaving large areas of northern temperate forest, boreal forest and tundra devoid of native earthworms. In these areas, invasions by L. rubellus take place in unoccupied soils (e.g. Alban and Berry, 1994; Frelich et al., 2006).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

AfghanistanPresentIntroducedGates, 1972
ArmeniaPresentIntroducedGates, 1972
AzerbaijanPresentIntroducedGates, 1972
ChinaPresentIntroducedGates, 1972
Georgia (Republic of)PresentGates, 1972
IndiaPresentPresent based on regional distribution.
-Andaman and Nicobar IslandsPresentIntroducedGates, 1972Nicobar Island
JapanPresentIntroducedGates, 1972
KazakhstanPresentIntroducedGates, 1972
TurkeyPresentIntroducedGates, 1972
TurkmenistanPresentIntroducedGates, 1972

Africa

South AfricaPresentIntroducedGates, 1972

North America

CanadaPresentIntroduced Invasive Gates, 1972
-British ColumbiaPresentIntroducedGates, 1972
-New BrunswickPresentIntroduced Invasive Gates, 1972
-Newfoundland and LabradorPresentIntroducedGates, 1972
-Nova ScotiaPresentIntroduced Invasive
-OntarioPresentIntroduced Invasive Gates, 1972
-QuebecPresentIntroduced Invasive Gates, 1972
GreenlandPresentIntroducedGates, 1972
USAPresentIntroduced Invasive Gates, 1972
-AlaskaPresentIntroducedGates, 1972; Costello et al., 2011
-ArkansasPresentIntroducedGates, 1972
-CaliforniaPresentIntroducedGates, 1972
-IllinoisPresentIntroduced Invasive Gates, 1972
-IndianaPresentIntroduced Invasive Gates, 1972
-MainePresentIntroducedGates, 1972
-MassachusettsPresentIntroducedGates, 1972
-MichiganPresentIntroducedGates, 1972; Greiner et al., 2012
-MinnesotaHale et al., 2005a; Hale et al., 2005b
-MissouriPresentIntroduced Invasive Gates, 1972
-New HampshirePresentIntroduced Invasive Gates, 1972
-New JerseyPresentIntroduced Invasive Gates, 1972
-New YorkPresentIntroduced Invasive Gates, 1972
-OhioPresentIntroduced Invasive Gates, 1972
-OregonPresentIntroduced Invasive Gates, 1972
-PennsylvaniaPresentIntroduced Invasive Gates, 1972
-WashingtonPresentIntroduced Invasive Gates, 1972

South America

ChilePresentIntroducedZicsi and Csuzdi, 2001
ColombiaPresentIntroducedFeijoo et al., 2004

Europe

AustriaPresentNativeGates, 1972
BelarusPresentIntroducedCAB ABSTRACTS Data Mining 2001; Gates, 1972
BelgiumPresentIntroducedGates, 1972
Bosnia-HercegovinaPresentIntroducedGates, 1972
BulgariaPresentIntroducedGates, 1972
CroatiaPresentIntroducedGates, 1972
Czech RepublicPresentIntroducedGates, 1972
Czechoslovakia (former)PresentIntroducedGates, 1972
DenmarkPresentIntroducedGates, 1972
EstoniaPresentIntroducedGates, 1972
Faroe IslandsPresentIntroducedGates, 1972
FinlandPresentIntroducedGates, 1972
FrancePresentIntroducedGates, 1972
-CorsicaPresentIntroducedGates, 1972
GermanyPresentIntroducedGates, 1982Possibly native also
GreecePresentIntroducedGates, 1972
HungaryPresentIntroducedGates, 1972Possibly native also
ItalyPresentIntroducedGates, 1972Possibly native also
LatviaPresentIntroducedGates, 1972
LithuaniaPresentIntroducedGates, 1972
MacedoniaPresentIntroducedGates, 1972
NetherlandsPresentIntroducedGates, 1972
NorwayPresentIntroducedGates, 1972
PolandPresentIntroducedGates, 1972
PortugalPresentIntroducedGates, 1972
RomaniaPresentIntroducedGates, 1972
Russian FederationPresentIntroducedGates, 1972
-Central RussiaPresentIntroducedGates, 1972
-Southern RussiaPresentIntroduced
-Western SiberiaPresentIntroducedGates, 1972
SerbiaPresentIntroducedGates, 1972
SlovakiaPresentIntroducedGates, 1972
SloveniaPresentIntroducedGates, 1972
SpainPresentPresent based on regional distribution.
-Balearic IslandsPresentIntroducedGates, 1972
SwedenPresentIntroducedGates, 1972
SwitzerlandPresentIntroducedGates, 1972
UKPresentIntroducedGates, 1972
UkrainePresentIntroducedGates, 1972
Yugoslavia (former)PresentIntroducedGates, 1972
Yugoslavia (Serbia and Montenegro)PresentIntroducedGates, 1972

Oceania

New ZealandPresentIntroduced Invasive Lee, 1959

History of Introduction and Spread

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Earthworms were probably introduced historically via the horticulture trade, the practice of using earth as ballast in ships during the 16th-19th centuries, and the introduction of plants to newly colonized regions.

It was not until the 19th century that naturalists, including earthworm specialists, began to take note of the earthworms present in various regions. In this regard it is important to recall that until Savigny (1826), the scientific community regarded all earthworms as being of one species, L. terrestris. The pace of species discovery did not accelerate much until the late 19th century, by which time it became possible to make intelligent statements about earthworm natural distributions. Only then could a species be said to occur inside or outside its natural range (James, 2004).

As biological surveys in the late 19th and early 20th centuries began to reveal biogeographic and evolutionary patterns of terrestrial oligochaetes, it was noted that several earthworm species had distributions well beyond their expected native ranges, and were possibly displacing indigenous fauna in their introduced ranges (Eisen, 1900; Michaelsen, 1900; Beddard, 1912). Michaelsen (1900) wrote that many species were 'widely transported'. Over the following century there has been a steady accumulation of evidence of earthworm introductions worldwide (e.g. Stebbings, 1962; Ljungstrom, 1972; Gates, 1972; 1982).

Gates (1972; 1982) monitored earthworms intercepted with imported plants and soils quarantined by the US Department of Agriculture over a 32-year period (1950-1982), and found that earthworms from all over the world were continually being imported into the US.

Risk of Introduction

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L. rubellus has a high risk of being introduced into more locations because it is commercially exploited and used as fishing bait. In Europe and North America it is already so widespread that additional introductions will have little impact; however, there is still the risk of introduction in remote sites where recreational fishing is possible.

Northeast Asia, including Japan, northern China, Korea, and far eastern Russia, could also experience invasions of L. rubellus.

Temperate regions in the southern hemisphere are already populated to a degree, but more locations could be invaded. Except in the broadly glaciated areas of Chile, Argentina and New Zealand, there are indigenous species of earthworms which could either resist L. rubellus invasions or risk being reduced in numbers by such invasions.

Habitat

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Adapted from ISSG (2013):

L. rubellus is common in coniferous forests in its native European and introduced North American range (Addison, 2009). It is found in relatively high organic matter horizons of the soil-litter complex, although it can also occur in humid regions with other vegetation types where the organic matter content of soils is abundant and/or a litter layer develops (Gates, 1972; Blakemore, 2006). It has also been documented to thrive in riparian zones characterized by high soil moisture and compacted soils, thought to present challenging conditions for earthworms (Costello and Lamberti, 2008).

It feeds on the surface litter but also burrows and produces casts in the upper mineral soil layer, and is found intimately associated with plant roots, suggesting that this species actively feeds in the rhizosphere (Hale et al., 2008). It is relatively frost tolerant (Tiunov et al., 2006), and thrives in soils with low pH (range 3.0-7.7) (Wironen and Moore, 2006).

Troglophilic (cave-dwelling) behaviour has been observed in L. rubellus in Alabama, Georgia, South Carolina and Tennessee (Reeves et al., 1999).

Habitat List

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CategoryHabitatPresenceStatus
Terrestrial-managed
Cultivated / agricultural land Present, no further details Natural
Disturbed areas Present, no further details Natural
Industrial / intensive livestock production systems Present, no further details Natural
Managed forests, plantations and orchards Present, no further details Natural
Managed grasslands (grazing systems) Present, no further details Natural
Rail / roadsides Present, no further details Natural
Urban / peri-urban areas Present, no further details Natural
Terrestrial-natural/semi-natural
Natural forests Present, no further details Harmful (pest or invasive)
Natural grasslands Present, no further details Natural
Riverbanks Present, no further details Natural

Biology and Ecology

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Genetics

n=36, diploid. There are no known hybrids with other species.

Reproductive Biology

L.rubellus is a hermaphrodite, with obligate out-crossing. Copulation takes place in the soil, during which sperm is exchanged between individuals and stored in the spermathecae of the recipient. Fertilization occurs later, after egg capsules (cocoons) are formed on the clitellum. Developing cocoons are supplied with nutritional material to support embryo growth. The ova are quite small, and as the cocoon slides off towards the head end, the ova are deposited in the cocoon via the female pores on segment 14, and then sperm stored in spermathecae are placed in the cocoon. Fertilization takes place in the cocoon, and the cocoon is deposited in a small chamber in the soil. After several weeks the young worms emerge and begin feeding in the soil. In the early juvenile state the worms do not form the vertical burrows characteristic of adults. Adulthood probably requires a minimum of one year's growth, with reproductive maturity attained in the second year.

Physiology and Phenology

Breeding takes place in the damper periods of the year, most commonly in spring and early summer in cooler climates. Activity is limited by moisture and temperature. High soil and night air temperatures inhibit activity, as do low night atmospheric humidity and dry soil. During such times (mainly summer) the worms will retreat to deeper soil. Winter temperatures can also limit activity, though in maritime climates activity can continue through the winter.

Nutrition

L. rubellus feeds on humified plant remains and A-horizon mineral soil.

Climate

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ClimateStatusDescriptionRemark
Cf - Warm temperate climate, wet all year Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Df - Continental climate, wet all year Preferred Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)
Ds - Continental climate with dry summer Preferred Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)
Dw - Continental climate with dry winter Preferred Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Talpa europaea Predator Larvae

Notes on Natural Enemies

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Various vertebrates are known to eat L. rubellus and other earthworms. Pigs (both feral and native species), foxes, moles, shrews, some birds (Bengtson et al., 1978) and salmonids (Costello et al., 2011) may all eat worms when available. None are potential control agents. Invertebrate predators include some predatory beetles (Carabidae; Harper et al., 2005), flatworms of the genera Australoplana and Arthurdendyus (Blackshaw, 1997; Santoro and Jones, 2001), and perhaps some centipedes (scolopendromorphs) and dipteran larvae (Tabanidae).

Means of Movement and Dispersal

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Natural Dispersal (Non-Biotic)

Individuals move on the soil surface or within the soil as a result of burrowing. The highest rate of natural dispersal is achieved during rainfall, when worms leave their burrows and crawl apparently aimlessly on the surface. Eventually they may find cover and form new burrows, or they may die from exposure to too much sunlight and drying, or to predators. This is essentially a process of diffusion, so worms are equally likely to travel into areas of established populations or areas free of other individuals of their species. However, because they are obligately biparental, a single individual cannot found a new population unless that individual has received sperm in copulation prior to dispersal. It is possible that some water-borne dispersal takes place, if the water into which the worms fall is not moving too fast and they can find a way to climb out. Riparian areas downstream of timber harvesting may be particularly at risk from water-borne dispersal (Costello et al., 2011). All natural dispersal is local and not long distance.

Accidental Introduction

The most common means of transport is accidental inclusion in soils, plant pots, mulches or other materials moved by people in the agricultural and horticultural trades. Discarding of bait also spreads L. rubellus. Logging, back-country fishing and off-road recreation (using either pack animals and motorized vehicles) are significant transport vectors into remote areas (Hale et al., 2005a,b; Holdsworth, 2007a,b; Costello et al., 2011). Accidental introductions can be local, national or international, as indicated by the fact that the species has crossed many international and inter-continental boundaries.

Intentional Introduction

These worms may be intentionally introduced as part of soil bioremediation efforts and also to establish new populations for use as fishing bait. Such transport can be local, national or international.

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aquaculture stock Yes Yes
Mulch, straw, baskets and sod Yes
Soil, sand and gravel Yes Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Growing medium accompanying plants adults; eggs; juveniles Yes Pest or symptoms usually visible to the naked eye

Impact Summary

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CategoryImpact
Cultural/amenity Negative
Economic/livelihood Positive and negative
Environment (generally) Positive and negative

Economic Impact

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There is some use of this species as fishing bait but the size of the market is unknown.

Environmental Impact

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Impact on Habitats

Forest floor habitats can be extensively altered by the combined action of L. rubellus and other invasive earthworms (Alban and Berry, 1994; Bohlen et al., 2004; Hale et al., 2005a,b; Suárez et al., 2006). In Minnesota hardwood forests the effect of any one species is less than the combined effect of three species, including L. rubellus, L. terrestris and one other (Hale et al., 2008).

The native state in areas without natural earthworm populations is to develop thick leaf mats on the forest floor, in which various other soil invertebrates live. With the introduction of earthworm species, litter layers are rapidly reduced to humified organic matter and mixed with mineral soil. The physical soil environment and soil chemistry is modified. Dramatic changes in forest soil profiles were caused by exotic European lumbricid earthworms in Australia and North America (e.g. Nielsen and Hole, 1964; Abbott, 1985; Alban and Berry, 1994; Scheu and Parkinson, 1994). Changes in nutrient dynamics and forest floor plant communities could have long-term effects on forest productivity (Hale et al., 2008). It is speculative to estimate these without further study.

Impact on Biodiversity

The change in the structure, microbial community content and chemistry of the forest floor caused by introduced L. rubellus can be profound (Eisenhauer et al., 2007) and is expected to affect soil invertebrates. Plant communities are also affected (Holdsworth et al., 2007a,b), with reduced diversity of the forest floor herb layer and the promotion of some invasive plants.

By consuming the leaf litter layer in North American hardwood forests, which established in the absence of earthworms, L. rubellus has been associated with a decline in herbaceous ground plants in Minnesota and Wisconsin (Loss et al., 2012). The loss of these ground plants and their replacement by sedges and grasses correlates with reduced ovenbird (Seiurus aurocapilla) and hermit thrush (Catharus guttatus) densities in sugar maple/basswood (Tilia americana) woodland, and with reduced ovenbird nesting success. Other birds, and other types of hardwood forest, appear unaffected.

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
  • Tolerant of shade
  • Capable of securing and ingesting a wide range of food
  • Highly mobile locally
  • Benefits from human association (i.e. it is a human commensal)
  • Fast growing
  • Has high reproductive potential
Impact outcomes
  • Altered trophic level
  • Damaged ecosystem services
  • Ecosystem change/ habitat alteration
  • Increases vulnerability to invasions
  • Modification of successional patterns
  • Negatively impacts forestry
  • Reduced amenity values
  • Reduced native biodiversity
  • Threat to/ loss of endangered species
  • Threat to/ loss of native species
Impact mechanisms
  • Competition - monopolizing resources
  • Competition
  • Interaction with other invasive species
  • Rooting
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Highly likely to be transported internationally deliberately
  • Difficult/costly to control

Uses

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L. rubellus is used as fishing bait and in compost.

Environmental Services

Earthworms are ecosystem engineers with diverse physical and chemical effects on soils (Lee, 1985). Taking a positive view of the environmental impact of L. rubellus and other invasive earthworms, it can be said that they occupy a key role in nutrient cycling and in the movement of air and water within soils.

However, where an ecosystem has developed in the absence of earthworms, existing communities and ecological relationships can be disrupted by the arrival of L. rubellus or other species. See Environmental Impacts.

Uses List

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Animal feed, fodder, forage

  • Bait/attractant

Environmental

  • Agroforestry
  • Revegetation

General

  • Laboratory use
  • Sport (hunting, shooting, fishing, racing)

Detection and Inspection

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Digging and hand-sorting of topsoil is an effective means of collecting L. rubellus. It can often be found in or under quantities of forest organic matter.

L. rubellus can also be collected with mustard powder suspension in water, applied to the soil in volumes of about 20 liters per 0.5 m2, or a suspension of 150 ml pureed strong onion in 10 L of water (G Steffen, unpublished data). These suspensions irritate most earthworms and causes them to leave the soil. They are particularly effective on epigeic or epi-endogeic species living in the topsoil and soil-litter interface.

Greiner et al. (2011) used electricity to extract L. rubellus.

Similarities to Other Species/Conditions

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L. rubellus and L. castaneus (Savigny, 1826) overlap in body size, the latter being usually smaller and having a darker, browner pigmentation. These and other species of Lumbricus can be distinguished by external features, such as the position of the clitellum, position and form of the tubercula pubertatis and other genital markings, size, colouring, and tail morphology.

L.rubellus has two genetically divergent lineages that are not distinguished by any morphological characters. The divergence was discovered with DNA barcodes, and further research is needed to check the two lineages for morphological differences. In addition, it is important to determine which lineage corresponds to the nominal species, based on the type material and/or topotypical material which could be collected from the type location. Eventually it may prove that what we currently understand to be L. rubellus must be split into two species (or subspecies), one of them retaining the name L. rubellus and the other taking a different name. The latter could depend on lineage matching to any junior synonyms of L. rubellus.

Prevention and Control

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Public Awareness

Education campaigns may be effective in reducing the discarding of fishing bait, and thereby reducing one of the means of long-distance transportation of L. rubellus. Other vectors, such as the horticultural and nursery trade, could be similarly limited. However, most people consider earthworms to be beneficial to landscape plants, so cooperation could be difficult.

Cultural Control and Sanitary Measures

Elimination of populations in sources of landscaping plants, mulches, and composts is a potentially effective means of preventing spread.

Biological Control

There are no known effective biological control agents except by other exotic species; certain flatworms are capable of reducing earthworm populations (Jones et al., 2001). The control agent and L. rubellus may establish wildly oscillating population cycles.

Chemical Control

Chemicle control is possible but the effective chemicals are potent biocides with wide non-target effects on humans and wildlife.

Control by Utilization

Collecting L. rubellus as bait is not practiced, because there are no economically effective means of gathering large numbers.

Gaps in Knowledge/Research Needs

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More research is needed into the ecological impacts of L. rubellus, including interactions with native species (both earthworms and other species), nutrient cycling and plant dynamics. There is a need to investigate lineage diversity and the ecological qualities of the various lineages, including factors related to invasiveness; to test the effectiveness of molecular identification techniques (e.g. DNA barcoding) on the various lineages of L. rubellus; to study the degree to which this species is used as fishing bait, and the potential economic impact of restricting the sale of this worm species.

References

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Abbott I, 1985. Distribution of introduced earthworms in the Northern Jarrah Forest of Western Australia. Australian journal of Soil Research, 23:263-70.

Addison JA, 2009. Distribution and impacts of invasive earthworms in Canadian forest ecosystems. Biological Invasions, 11(1):59-79. http://www.springerlink.com/content/5n05842303n68146/?p=f4036f1517dd4ab1a6961f73b8fb7d2f&pi=4

Alban DH; Berry EC, 1994. Effects of earthworm invasion on morphology, carbon, and nitrogen of a forest soil. Applied Soil Ecology, 1:243-249.

Beddard FE; 1912, republ. 2011. Earthworms and their allies [ed. by Beddard, F. E.]. Cambridge, UK: Cambridge University Press, 150 pp.

Bengtson SA; Rundgren S; Nilsson A; Nordstrom S, 1978. Selective predation on lumbricids by golden plover Pluvialis apricaria. Oikos, 31(2):164-168.

Blackshaw RP, 1997. The planarian Artioposthia triangulata (Dendy) feeding on earthworms in soil columns. In: Soil Biology & Biochemistry, 29(3/4) [ed. by Edwards, C. A.]. 299-302.

Blakemore RJ, 2006. Cosmopolitan earthworms - an eco-axonomic guide to the peregrine species of the world., Japan: VermEcology, 600 pp.

Bohlen PJ; Scheu S; Hale CM; McLean MA; Migge S; Groffman PM; Parkinson D, 2004. Non-native invasive earthworms as agents of change in northern temperate forests. Frontiers in Ecology and the Environment, 2:427-435.

Bouche MB, 1972. Lombriciens de France; Ecologie et Systématique. Paris, France: INRA, 671 pp.

Burtelow AE; Bohlen PJ; Groffman PM, 1998. Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States. In: Applied Soil Ecology, 9(1/3). 197-202.

Costello DM; Lamberti GA, 2008. Non-native earthworms in riparian soils increase nitrogen flux into adjacent aquatic ecosystems. Oecologia, 158(3):499-510. http://springerlink.metapress.com/content/a4m8777384n054h6/fulltext.html

Costello DM; Tiegs SD; Lamberti GA, 2011. Do non-native earthworms in Southeast Alaska use streams as invasional corridors in watersheds harvested for timber? Biological Invasions, 13(1):177-187. http://www.springerlink.com/content/d346107712501207/

Edwards CA, 2004. Earthworm ecology. 2nd edition. Boca Raton, USA: CRC Press, 448 pp.

Eisen G, 1900. Researches in American Oligochaeta, with especial reference to those to the Pacific Coast and adjacent islands. Proceedings of the California Academy of Science, 3rd Series, Zoology, 2:85-276.

Eisenhauer N; Partsch S; Parkinson D; Scheu S, 2007. Invasion of a deciduous forest by earthworms: changes in soil chemistry, microflora, microarthropods and vegetation. Soil Biology & Biochemistry, 39(5):1099-1110. http://www.sciencedirect.co./science/journal/00380717

Feijoo AV; Quintero HV; Fragoso C; Moreno AG, 2004. Patrón de distribución y listado de especies de las lombrices de tierra (Annelida: Oligochaeta) en Colombia. Acta Zoologica Mexicana (n.s.), 20(2):197-220.

Frelich LE; Hale CM; Scheu S; Holdsworth AR; Heneghan L; Bohlen PJ; Reich PB, 2006. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biological Invasions, 8(6):1235-1245. http://www.springerlink.com/content/a15131hpk7815521/fulltext.pdf

Gates GE, 1972. Burmese earthworms. An introduction to the systematics and biology of megadrile oligochaetes with special reference to southeast Asia. Transactions of the American Philosophical Society, 62(7). 326 pp.

Gates GE, 1982. Farewell to North American Megadriles. Megadrilogica, 4:12-77.

Greiner HG; Kashian DR; Tiegs SD, 2012. Impacts of invasive Asian (Amynthas hilgendorfi) and European (Lumbricus rubellus) earthworms in a North American temperate deciduous forest. Biological Invasions, 14(10):2017-2027. http://www.springerlink.com/content/r61p6h6625631576/

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