Lumbricus terrestris

Pictures

Picture	Title	Caption	Copyright
Title General view Caption Lumbricus terrestris; general view. Copyright Thibaud Decaens	General view	Lumbricus terrestris; general view.	Thibaud Decaens
Title Anterior Caption Lumbricus terrestris: close-up of anterior sections. Copyright Thibaud Decaens	Anterior	Lumbricus terrestris: close-up of anterior sections.	Thibaud Decaens
Title Posterior Caption Lumbricus terrestris: close-up of posterior sections. Copyright Thibaud Decaens	Posterior	Lumbricus terrestris: close-up of posterior sections.	Thibaud Decaens

Identity

Preferred Scientific Name

• Lumbricus terrestris L.

International Common Names

• English: lob worm; nightcrawler

Local Common Names

• UK: dew worm
• USA: dew worm

Summary of Invasiveness

The earthworm L. terrestris is thought to be native to Western Europe but it is now globally distributed in temperate to mild boreal climates. It is clearly an invasive species, even within parts of Europe that have indigenous earthworms of similar ecology. Furthermore, its invasive range includes northern Europe as there were no earthworms in glaciated areas. Most of the invasion can be attributed to human activity, such as the movement of plants and soils, and importantly, the transport of L. terrestris as fish bait (Tomlin, 1983; Hale et al., 2005). Once present in an environment, its activities can radically alter forest floor litter decomposition regimes and the soil-litter communities based on forest floor litter. It is considered invasive as it is widespread globally, tolerant to a range of transport and climatic conditions and, being a hermaphrodite, only two individuals are needed in a founding population. However, little is known about the properties which make this species so invasive. Invasiveness qualities of earthworms in general can be found in Hendrix et al. (2008). L. terrestris is listed on the Global Invasive Species Database (ISSG, 2013).

Taxonomic Tree

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

Notes on Taxonomy and Nomenclature

LumbricusterrestrisLinnaeus (1758) was the first earthworm given a name in the Linnaean system, but there was considerable debate about the identity of the worm, the validity of the name and other aspects of nomenclature because the description was extremely brief and no type specimen was deposited by Linnaeus. The morphologically identical worm EnterionherculeumSavigny (1826) was proposed by some to be the first validly established member of the genus Lumbricus, and the name L. herculeus was in favour with some taxonomists for quite some time (Tetry, 1937; Bouche, 1972). Several other names, now believed to be junior objective synonyms of L. terrestris, were also proposed. Designation of a neotype by Sims (1973) fixed the identity of L. terrestris. Sims (1973) followed the long tradition, at least since Michaelsen (1900), of regarding L. herculeus as a junior synonym of L. terrestris. This was in keeping with the morphological species concept in general use. James et al. (2010) discovered that there are two genetically distinct lineages within nominal L. terrestris, and that these corresponded to L. terrestris and L. herculeus, with the latter as a cryptic species, indistinguishable except by size differences. James et al. (2010) removed L. herculeus from the synonymy of L. terrestris and provided a simple molecular marker, the cytochrome oxidase subunit I DNA barcode (Hebert et al., 2003), which is both necessary and sufficient to identify the two species. DNA barcoding is quite effective on earthworms (Richard et al., 2009). The Sims (1973) neotype was determined to be lost, and has been replaced by a subsequent neotype designated in James et al. (2010). This current neotype has the advantage of being in preservative that does not destroy DNA, and the neotype has been DNA-barcoded.

The restriction of L. terrestris to a lineage first found in the Uppsala Botanical Garden in Sweden, but it also being found widely distributed in Europe and North America, means that much past work on L. terrestris could be unreliable. It is possible that L. herculeus was actually involved for many reported accounts of L. terrestris, or that it was a mix of both species.

Description

External Features

Length 110-200 mm, diameter 7-10 mm, segment number 120-170, mostly 135-150. Body cylindrical in cross section except for broad, flattened posterior. Head end dark brown to reddish brown 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 or 8/9; spermathecal pores lateral in furrows 9/10/11 between setae C and D level. Male pores on prominent pads in 15, clitellum 32-37, tubercular ridge 32 or 33- 36. Setae are closely paired, the ventral setae (A) more widely spaced than the ventral couple (A and B), the distance between B and C slightly less than the AA distance, and the CD distance slightly less than AB. Small papillae surround setae A and B on segments 25 and 26 (variable), and in the segments of the clitellum.

Internal Features

Septa present from 4/5; 6/7-9/10 strongly muscularized. Gizzard in 17-19, typhlosole begins in 21. Last pair of hearts in 11. Seminal vesicles in 9, 11 and 12; spermathecae in 9 and 10.

A detailed description of the adult stage can be found in Sims (1973).

Adults and juveniles are not reliably identifiable by any means other than molecular data, for which DNA barcode region is recommended. Cocoons (egg capsules) may be larger than those of most other earthworms in the same location, except where other large-bodied worms such as Aporrectodea longa occur. Therefore, cocoons cannot be reliably identified without molecular tools.

Distribution

After over 2000 years of human-mediated transportation, determining the native range for the common invasive earthworms of Europe seems an impossible task (Gates, 1972). The use of molecular techniques may help to identify its exact origin but requires extensive sampling of populations in western and central Europe. Potentially, the genus Lumbricus could range from the Pyrenees across France through Austria, Hungary and Romania, to southern Germany. L. terrestris is likely to be native to the western half of this range, considering that its occurrence in Romanian forests is relatively recent (Pop and Pop, 2006). The slightly smaller but otherwise almost identical L. herculeus is known mainly from France with invasive populations there and in Sweden. In Andorra there is another small morph with strong morphological resemblance to L. terrestrisand L. herculeus, but quite divergent in the cytochrome oxidase I DNA barcode gene region (SW James, unpublished data, 2013). These factors point to a central France-Pyrenees origin of Lumbricus species allied to L. terrestris.

Pleistocene glaciations are thought to have eliminated the earthworm fauna from most of the northern temperate regions of Earth (Tiunov et al., 2006). Natural refaunation by dispersal from southern glacial refugia in North America, Europe and Asia has been slow at about 10 m per year (Terhivuo and Saura, 2006), leaving large areas of north temperate forest, boreal forest and tundra devoid of native earthworms. In these areas, invasions take place in unoccupied soils (Alban and Berry, 1994; Frelich et al., 2006). 

It is likely that L. terrestris is sold for fish bait at least in all of the lower 48 States in the USA, and therefore probable that the species is present in small pockets in all but the hottest and driest of the States.

Distribution Table

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.

History of Introduction and Spread

Much speculation has been made about earthworm invasion history in general, but they were probably introduced historically via the horticulture trade, the practice of using earth as ballast in ships between the sixteenth and nineteenth centuries, and the introduction of plants to newly colonized regions. L.terrestris was first described from a population in Uppsala, Sweden in 1758 but it is likely that its introduction and spread to Europe occurred much earlier, before merchants and colonists took much recognition of the species. Due to this lack of interest and so a lack of reported information regarding the species movements, it is unlikely to have originated from Uppsala. It probably arrived in North America at or before this time, but further spread took place much later.

It was not until the nineteenth century that naturalists, including earthworm specialists, began to take note of the earthworms present in various areas. 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 nineteenth 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).

Michaelsen (1900) indicated that many species were “widely transported”, and the same species, and more, are recognized today as peregrine or invasive species. A good compilation of these is in Blakemore (2006). It was also noted that several earthworm species were possibly displacing indigenous fauna (Michaelsen, 1900; Eisen, 1900; Beddard, 1912). Over the ensuing century there has been a steady accumulation of evidence of earthworm introductions worldwide (Smith, 1928; Gates, 1972, 1982; Ljungstrom, 1972; Stebbings, 1962).

Smith (1928) noticed that L. terrestris invaded an urbanized area of central Illinois, USA, apparently displacing Diplocardia communis in the process.  Pop and Pop (2006) found L. terrestris in new locations in Romania in recent years, indicating on-going invasion of places with indigenous Romanian earthworms. Gates (1972) recounts anecdotal evidence of early twentieth century arrivals in parts of Ohio and Illinois, Washington, and North Carolina. In contrast, some kind of earthworm, possibly L. terrestris, was present in areas of Michigan, Utah, and Idaho by the mid to late nineteenth century.

Gates (1972, 1982) monitored oligochaetes 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. On a more local scale, back-country fishing and off-road recreation (pack animals and motorized vehicles) are significant vectors of transport into remote areas (Hale et al., 2005; Holdsworth, 2007).

Risk of Introduction

L. terrestis has a high risk of being introduced into more locations because it is commercially exploited and widely used as fishing bait, an educational resource and a model organism.  As the species is already so widespread in Europe and North America, the likelihood of additional introductions is small; 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 this species. 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. terrestris invasions, or risk being reduced in number by such invasions.

One should not believe that the absence of L. terrestris from a particular habitat within its climatic range is an indication that the site is safe from invasion. Räty (2004) found that experimental introduction of L. terrestris into acid forest soil was successful. Therefore the primary limiting factor of its distribution within the climate range could be access to sites. Self-propelled spread is slow at 6.3 m per year or about 6 km per 1000 years (Ligthart et al., 1997). This species is capable of moving 4-19 m in a single night (Mather and Christensen, 1988) but this is a random walk, not directed towards unoccupied areas. From these data one can conclude that the modern distribution of L. terrestris and the distributions of many other common invasive earthworms are largely the result of human activity.

On the other hand, not all deliberate introductions are successful (Butt et al., 1999). Thus the successful establishment of a new population whether accidental or deliberate, is not guaranteed from the mere arrival of the earthworms at a site. A variety of factors, such as time of year, weather, site characteristics, and condition of the propagules on arrival, may be determinants of successful establishment.

Habitat List

Biology and Ecology

Genetics

Chromosome number 36, diploid. There are no known hybrids with other species.

Reproductive Biology

L. terrestris is a hermaphrodite, with obligate outcrossing. Individuals seek mates of the largest size available resulting in similar-sized individuals actually copulating (Michiels et al., 2001). Copulation takes place on the soil surface at night, during which sperm is exchanged between individuals, and stored in the spermathecae of the recipient. Fertilization occurs later after cocoons (egg capsules) are formed on the clitellum. The developing cocoon is supplied with nutritional material to support embryo growth, the ova being quite small. As the cocoon slides off towards the head end, 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 adjacent to the parental burrow. 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 growth, with reproductive maturity attained in the second year.

Physiology and Phenology

Breeding takes place in damper periods of the year, most commonly 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 the deepest parts of their burrows. Winter temperatures can also limit activity, though in maritime climates activity can continue through the winter.

Nutrition

The earthworm feeds on dead leaves at the surface and A-horizon mineral soil.

Climate

Latitude/Altitude Ranges

Air Temperature

Rainfall

Rainfall Regime

Notes on Natural Enemies

Various vertebrates are known to eat L. terrestris and other earthworms. Pigs (both feral and native species), foxes, moles, shrews, and some birds (Bengtson et al., 1978), will eat worms when available. However, none are suitable as potential control agents. Invertebrate predators include some predatory beetles (Carabidae) (Harper et al., 2005), flatworms of the genera Australoplana and Arthurdendyus (Blackshaw, 1997; Jones et al., 2001; Santoro and Jones, 2001), and possibly some centipedes (Scolopendromorphs) and dipteran larvae (Tabanidae).

Means of Movement and Dispersal

Natural Dispersal (Non-Biotic)

Individuals move on the soil surface or within the soil as a result of burrowing (Ligthart et al., 1997). The highest rate of dispersal is achieved during rainfall when the worms leave their burrows and crawl apparently aimlessly on the surface (Mather and Christensen, 1988). Eventually they may find cover and form new burrows, or they may die from exposure to too much sunlight and drying out, 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 obligatory biparental, a single individual cannot establish a new population unless that individual has received sperm in copulation prior to dispersal. It is possible that some water-borne dispersal takes place, but only if the water that the worm has fallen into is not fast flowing and they are able to climb out. All natural dispersal is local and not long distance, averaging less than 10 m per year (Ligthart et al., 1997; Tiunov et al., 2006).

Accidental Introduction

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

Intentional Introduction

These worms may be deliberately introduced as part of soil bioremediation efforts and also to establish new populations for exploitation as fishing bait. Such transport can be local, national or international but introduction is not always successful (Butt et al., 1999).

Pathway Causes

Pathway Vectors

Plant Trade

Impact Summary

Environmental Impact

Impact on Habitats

During the last 100 years, dramatic changes in forest soil profiles caused by exotic European lumbricid earthworms have been reported in Australia and North America (Nielsen and Hole, 1964; Abbott, 1985; Alban and Berry, 1994; Scheu and Parkinson, 1994). Forest floor habitats can be extensively altered by the combined action of L. terrestris and other invasive earthworms (Hale et al., 2005a, b; Alban and Berry, 1994; Bohlen et al., 2004; 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). Litter layers are reduced rapidly to humified organic matter and mixed with mineral soil. 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.

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 is profound (Eisenhauer et al., 2007) and is expected to affect soil invertebrates. Plant communities are also affected (Holdsworth, 2007a, b) with reduced forest floor herb layer diversity and the promotion of some invasive plants.

Risk and Impact Factors

• Proved invasive outside its native range
• Highly adaptable to different environments
• Is a habitat generalist
• 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)
• Long lived

• 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

• Competition - monopolizing resources
• Competition
• Interaction with other invasive species
• Rooting

• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally deliberately
• Difficult/costly to control

Uses

Economic Value

There is a substantial fishing bait market in North America. Most of the supply is gathered manually from golf courses at night (Tomlin, 1983). 

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. terrestris and other invasive earthworms, it can be said that they perform a number of environmental services, including: modifying the physical soil environment, transforming organic matter and modifying soil chemistry. Earthworms often 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. terrestris or other species. See Environmental Impacts.

Uses List

Animal feed, fodder, forage

• Bait/attractant

Environmental

• Agroforestry
• Revegetation

General

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

Detection and Inspection

L. terrestris forms characteristic “middens” of dead leaf parts pulled into a burrow opening and mixed with faecal matter, which strongly resembles soil. Pulling gently will reveal a hole of about 5-6 mm in diameter. As other species of similar ecology create comparable formations, species presence must be confirmed by collecting adult specimens. This can be done at night when the animals emerge from their burrows to feed. Soil conditions must be moist and temperatures not much in excess of 20°C. Rain also aids emergence and collection. Juveniles can be caught more readily by digging and hand-sorting of the topsoil but they are more difficult to identify, except by molecular means. DNA barcodes are necessary for certain identification of L. terrestris. Daytime collection can be accomplished with mustard powder suspension in water, applied to the soil in volumes of about 20 L per 0.5 m², or a suspension of 150 ml pureed strong onion in 10 L of water (Steffen et al., 2013). These suspensions irritate most earthworms and cause them to leave the soil.

Similarities to Other Species/Conditions

L. herculeus and L. terrestris are morphologically identical, except for body size. L. terrestris is larger, but the size distributions for length, body mass and segment number overlap (James et al., 2010). Large individuals of L. terrestris can usually be distinguished from small individuals of L. herculeus by size alone, but the DNA barcode region sequence is the only reliable means of identification (James et al., 2010). The two species do co-occur in France, but are more commonly found separately. Regardless, a combination of measurements and DNA data should be used to unequivocally identify L. terrestris. Other species of Lumbricus can be distinguished by external characters such as position of the clitellum, position and form of the tubercula pubertatis and other genital markings, size, coloration, and tail morphology.

Prevention and Control

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. terrestris. 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, such as certain flatworms capable of reducing earthworm populations (Jones et al., 2001). The control agent and the target earthworms may establish wildly oscillating population cycles.

Chemical Control

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

Control by Utilization

Collection for bait is practiced on a large scale with this species but generally on mowed grasslands such as golf courses, where bait collectors can capture them efficiently. It will not be an effective method of control in other locations, such as forests, where the invasion problem is more severe.

Gaps in Knowledge/Research Needs

There is a need to investigate lineage diversity and the ecological qualities of the two similar species, L. terrestris and L. herculeus, including factors related to invasiveness, and 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. 

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22/12/10 Original text by:

S James, Consultant, USA

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