Earthworm

Life and physiology

At birth, earthworms emerge small but fully formed, lacking only their sex structures which develop in about 60 to 90 days. They attain full size in about one year. Scientists predict that the potential lifespan under field conditions is four to eight years, while the actual lifespan is probably no more than a few months because of intense predation and environmental hazards.

Reproduction

Several common earthworm species are mostly parthenogenetic, meaning that growth and development of embryos happens without fertilization. Among lumbricid earthworms, parthenogenesis arose during evolution from sexual relatives. Parthenogenesis in some Aporrectodea trapezoides lineages arose 6.4 to 1.1 million years ago from sexual ancestors. A few species exhibit pseudogamous parthogenesis, meaning that mating is necessary to stimulate reproduction, even though no male genetic material passes to the offspring.

Earthworm mating occurs on the surface, most often at night. Earthworms are hermaphrodites; that is, they have both male and female sexual organs. The sexual organs are located in segments 9 to 15. Earthworms have one or two pairs of testes contained within sacs. The two or four pairs of seminal vesicles produce, store and release the sperm via the male pores. Ovaries and oviducts in segment 13 release eggs via female pores on segment 14, while sperm is expelled from segment 15. One or more pairs of spermathecae are present in segments 9 and 10 (depending on the species) which are internal sacs that receive and store sperm from the other worm during copulation. As a result, segment 15 of one worm exudes sperm into segments 9 and 10 with its storage vesicles of its mate. Some species use external spermatophores for sperm transfer.

In Hormogaster samnitica and Hormogaster elisae transcriptome DNA libraries were sequenced and two sex pheromones, Attractin and Temptin, were detected in all tissue samples of both species. Sex pheromones are probably important in earthworms because they live in a concealed subterranean environment where chemical signalling may play a crucial role in attracting a partner and in facilitating outcrossing. Outcrossing would provide the benefit of masking the expression of deleterious recessive mutations in progeny. (see Complementation).

Copulation and reproduction are separate processes in earthworms. The mating pair overlap front ends ventrally and each exchanges sperm with the other. The clitellum becomes very reddish to pinkish in colour. Sometime after copulation, long after the worms have separated, the clitellum (behind the spermathecae) secretes material which forms a ring around the worm. The worm then backs out of the ring, and as it does so, it injects its own eggs and the other worm's sperm into it. Thus each worm becomes the genetic father of some of their offspring (due to its own sperm transferred to other earthworm) and the genetic mother (offsprings from its own egg cells) of the rest. As the worm slips out of the ring, the ends of the cocoon seal to form a vaguely onion-shaped incubator (cocoon) in which the embryonic worms develop. Hence fertilization is external. The cocoon is then deposited in the soil. After three weeks, 2 to 20 offspring hatch with an average of four. Development is direct that is without formation of any larva.

DNA repair

Exposure of the earthworm Eisenia fetida to ionizing radiation induced DNA strand breaks and oxidized DNA bases. These DNA damages could then be repaired in somatic and spermatogenic cells. Earthworm testis cells are also capable of repairing hydrogen peroxide induced oxidative DNA adducts.

Locomotion

Earthworms travel underground by means of waves of muscular contractions which alternately shorten and lengthen the body (peristalsis). The shortened part is anchored to the surrounding soil by tiny clawlike bristles (setae) set along its segmented length. In all the body segments except the first, last and clitellum, there is a ring of S-shaped setae embedded in the epidermal pit of each segment (perichaetine arrangement). The whole burrowing process is aided by the secretion of lubricating mucus. As a result of their movement through their lubricated tunnels, worms can make gurgling noises underground when disturbed. Earthworms move through soil by several means, depending on species and soil mechanical resistance, either by ingesting it, using root channels or by expanding crevices with force; when forces are measured according to body weight, hatchlings can push 500 times their own body weight whereas large adults can push only 10 times their own body weight.

Regeneration

Earthworm adults have the ability to regenerate lost segments, but this ability varies between species and the extent of damage as well as genetic factors within the same species. Earthworm regeneration is known from the 17th century, but the cellular mechanisms in play remain incompletetly understood. Regeneration involves epimorphosis, i.e. dedifferentiation of extant tissues followed by generation of new body tissues. The first stage of regeneration after an injury (mostly caused by a predator or agricultural machinery) is wound healing, followed by cell death, formation of a blastema and stem cell proliferation while mechanisms help the newly regenerated segments to determine polarity and positional identity within the body. It has been shown that regeneration takes place only in the presence of an intact clitellum. Earthworms are able to regenerate both anterior (head with brain included) and posterior segments, the intestine participating in head regeneration.

Earthworm extracts have been used for thousand of years as a traditional Chinese medicine for wound healing, and their efficacy has been attested by a recent meta-analysis of 16 published human and animal model studies.

Taxonomy and distribution

Within the world of taxonomy, the stable 'Classical System' of Michaelsen (1900) and Stephenson (1930) was gradually eroded by the controversy over how to classify earthworms, such that Fender and McKey-Fender (1990) went so far as to say, "The family-level classification of the megascolecid earthworms is in chaos." Over the years, many scientists have developed their own classification systems for earthworms, which led to confusion, and these systems have been and still continue to be revised and updated. The classification system used here which was developed by Blakemore (2000), is a modern reversion to the Classical System that is historically proven and widely accepted.

Categorization of a megadrile earthworm into one of its taxonomic families under suborders Lumbricina and Moniligastrida is based on such features as the makeup of the clitellum, the location and disposition of the sex features (pores, prostatic glands, etc.), number of gizzards, and body shape. Currently, over than 6,000 species of terrestrial earthworms are named, as provided in a species name database, but the number of synonyms is unknown.

The families, with their known distributions or origins:

• Acanthodrilidae
• Ailoscolecidae – the Pyrenees and the Southeastern United States
• Almidae – tropical equatorial (South America, Africa, Indo-Asia)
• Benhamiinae – Ethiopian, Neotropical (a possible subfamily of Octochaetidae)
• Criodrilidae – southwestern Palaearctic: Europe, Middle East, Russia and Siberia to Pacific coast; Japan (Biwadrilus); mainly aquatic
• Diplocardiinae – Gondwanan or Laurasian? (subfamily of Acanthodrilidae)
• Enchytraeidae – cosmopolitan but uncommon in tropics (usually classed with Microdriles)
• Eudrilidae – Tropical Africa south of the Sahara
• Exxidae – Neotropical: Central America and the Caribbean
• Glossoscolecidae – Neotropical: Central and South America, Caribbean
• Haplotaxidae – cosmopolitan distribution (usually classed with Microdriles)
• Hormogastridae – Mediterranean
• Kynotidae – Malagasian: Madagascar
• Lumbricidae – Holarctic: North America, Europe, Middle East, Central Asia to Japan
• Lutodrilidae – Louisiana, in the Southeastern United States
• Megascolecidae
• Microchaetidae – Terrestrial in Africa especially South African grasslands
• Moniligastridae – Oriental and Indian subregion
• Ocnerodrilidae – Neotropics, Africa; India
• Octochaetidae – Australasian, Indian, Oriental, Ethiopian, Neotropical
• Octochaetidae – Australasian, Indian, Oriental (subfamily if Benhamiinae is accepted)
• Sparganophilidae – Nearctic, Neotropical: North and Central America
• Tumakidae – Colombia, South America

As an invasive species

From a total of around 7,000 species, only about 150 species are widely distributed around the world. These are the peregrine or cosmopolitan earthworms. Of the 308 taxa of earthworms found in the United States and Canada, 70 (23%) are introduced species.

Ecology

Earthworms are classified into three main ecophysiological categories: (1) leaf litter- or compost-dwelling worms that are nonburrowing, live at the soil-litter interface and eat decomposing organic matter (epigeic) e.g. Eisenia fetida; (2) topsoil- or subsoil-dwelling worms that feed on soil, burrow and cast within the soil, creating horizontal burrows in upper 10–30 cm of soil (endogeic); and (3) worms that construct permanent deep vertical burrows which they use to visit the surface to obtain plant material for food, such as leaves (anecic, meaning "reaching up"), e.g. Lumbricus terrestris.

Earthworm populations depend on both physical and chemical properties of the soil, such as temperature, moisture, pH, salts, aeration, and texture, as well as available food, competition, predation, and the ability of the species to reproduce and disperse. One of the most important environmental factors is pH, but earthworms vary in their pH preferences, and through their engineering activities (summarized in the formation of earthworm mull humus) they are able to change pH in order to adapt it to their niche requirements (see niche construction and extended phenotype). Most favour neutral to slightly acidic soils. However, Lumbricus terrestris is still present in a pH of 5.4, Dendrobaena octaedra at a pH of 4.3 and some Megascolecidae are present in extremely acidic humic soils. Soil pH may also influence the numbers of worms that go into diapause. The more acidic the soil, the sooner worms go into diapause, and remain in diapause the longest time at a pH of 6.4.

Earthworms are preyed upon by many species of birds (e.g. robins, starlings, thrushes, gulls, crows), snakes, wood turtles, mammals (e.g. bears, boars, foxes, hedgehogs, pigs, moles) and invertebrates (e.g. ants, flatworms, ground beetles, centipedes, snails, and spiders). Earthworms have many internal parasites, including fungi, protozoa, platyhelminthes, mites, and nematodes; they can be found in the worms' blood, seminal vesicles, coelom, intestine, or in their cocoons.)

The earthworm activity aerates and mixes the soil (bioturbation), and is conducive to mineralization of nutrients and their uptake by vegetation together with incorporating organic matter and linking it to soil minerals. Certain species of earthworm come to the surface and graze on the higher concentrations of organic matter present there, mixing it with the mineral soil (anecic earthworms). Because a high level of organic matter mixing is associated with soil fertility, an abundance of earthworms is generally considered beneficial by farmers and gardeners. As long ago as 1881 Charles Darwin wrote: "It may be doubted whether there are many other animals which have played so important a part in the history of the world, as have these lowly organized creatures." It has long been debated whether earthworms contribute to the disappearance of organic matter in the form of carbon dioxide and mineral nutrients or rather to its preservation in the form of humus. Although these are both aspects of earthworm activities the net effect is important to ascertain, in particular in the frame of organic matter disappearance linked to global warming. It seems that there is now a consensus about the prominent role of earthworms in carbon sequestration due to the fact that part of organic matter is mineralized at or near the soil surface while the major part is incorporated in the deep soil where it is stabilized by links with clay minerals.

While the main habitat of earthworms is in soil, they are not restricted to this habitat. The brandling worm Eisenia fetida lives in decaying plant matter and manure. Arctiostrotus vancouverensis from Vancouver Island and the Olympic Peninsula is generally found in decaying conifer logs. Aporrectodea limicola, Sparganophilus spp., and several others are found in mud in streams (riparian species). Some species are arboreal, some aquatic and some euryhaline (salt-water tolerant) and littoral (living on the sea-shore), e.g. Pontodrilus litoralis. Even in the soil species, special habitats, such as ultramafic soils derived from serpentine, have an earthworm fauna of their own, e.g. New Caledonian Acanthodrilidae.

Vermicomposting of organic wastes is currently processed using the epigeic Eisenia fetida and Eisenia andrei which are particularly adapted to the consumption of fresh organic matter without deepening in the substrate (contrary to the anecis Lumbricus terrestris) and which tolerate the heat generated in compost heaps. Addition of this humified organic matter to the soil, preferably as a surface mulch, will improve moisture and nutrient availability, with beneficial effects on the soil microflora. It will also provide several species of earthworms with their food and nutrient requirements, and will create the optimum conditions of temperature and moisture that will stimulate their activity, although to a lesser extent than bacterial-mediated compost.

Earthworms are environmental indicators of soil health. Earthworms feed on the decaying matter in the soil and analyzing the microbial contents of their digestive tracts (the earthworm microbiome) gives insight into the overall condition of the soil. The earthworm gut bioaccumulates heavy metals and persistent organic pollutants, causing major health problems, but its microbiome promotes the degradation of many organic pollutants. The population size of earthworms indicates soil quality, as healthy soil would contain a larger number and biomass of earthworms, in particular endogeic and anecic species.

Environmental impacts

The major benefits of earthworm activities to soil fertility for agriculture can be summarized as:

• Biological: In many soils, earthworms play a major role in the conversion of large pieces of organic matter into rich humus, thus improving soil fertility. This is achieved by the worm's actions (mainly of anecics) of pulling below the surface deposited organic matter such as leaf fall or manure, either for food or to plug its burrow. Once in the burrow, the worm will shred the leaf, partially digest it and mingle it with the earth. Worm casts (see bottom right) can contain 40 percent more humus than the top 9 inches (230 mm) of soil in which the worm is living.

• Chemical: In addition to dead organic matter, the earthworm also ingests any other soil particles that are small enough, including sand grains up to 1⁄20 inch (1.3 mm), into its gizzard, wherein those minute fragments of grit (gastroliths) grind everything into a fine paste which is then digested in the intestine, increased surface area favouring microbial colonization and enzymatic action. When the worm excretes this paste in the form of casts, deposited on the surface or deeper in the soil, carbon, nitrogen and phosphorus are increased compared to the bulk soil and nutrients are changed to a plant-available form, increasing locally soil fertility. In conditions where humus is plentiful, the weight of casts produced may be greater than 4.5 kilograms (9.9 lb) per worm per year.
• Physical: The earthworm's burrowing creates a multitude of channels through the soil and is of great value in maintaining the soil structure, enabling processes of aeration and drainage. Permaculture co-founder Bill Mollison points out that by sliding in their tunnels, earthworms "act as an innumerable army of pistons pumping air in and out of the soils on a 24-hour cycle (more rapidly at night)". Thus, the earthworm not only creates passages for air and water to traverse the soil, i.e. increases soil porosity, but also as a soil engineer its bioturbation activities modify the vital organic component that makes a soil healthy. Earthworms promote the formation of nutrient-rich casts that have high soil aggregation (good soil structure) and soil fertility and quality. In podzol soils, after conversion of softwood to hardwood forest or after earthworm invasion, these animals can obliterate the characteristic banded appearance of the soil profile by mixing the organic (LFH), eluvial (E) and upper illuvial (B) horizonss to create a single dark Ap horizon.

Earthworms accelerate nutrient cycling in the soil-plant system through fragmention and mixing, physical grinding and chemical digestion of plant debris. However, the earthworm's existence cannot be taken for granted. Dr. W. E. Shewell-Cooper observed "tremendous numerical differences between adjacent gardens", and worm populations are affected by a host of environmental factors, many of which can be influenced by good management practices on the part of the gardener or farmer.

Darwin estimated that arable land contains up to 53,000 per acre (130,000/ha) of worms, but more recent research has produced figures suggesting that even poor soil may support 250,000 per acre (620,000/ha), whilst rich fertile farmland may have up to 1,750,000 per acre (4,300,000/ha), meaning that the weight of earthworms beneath a farmer's soil could be greater than that of the livestock upon its surface. Richly organic topsoil populations of earthworms are much higher, averaging 500 per square metre (46/sq ft) and up to 400 g/m2, such that, for the 7 billion of us, each person alive today has support of 7 million earthworms.

The ability to break down organic materials and excrete concentrated nutrients makes the earthworm a functional contributor in restoration projects. In response to ecosystem disturbances, some sites have utilized earthworms to prepare soil for the return of native flora. Research from the Station d'écologie Tropicale de Lamto (Ivory Coast) asserts that the earthworms positively influence the rate of macroaggregate formation (Soil structure#Granular|granular structure), an important feature for soil structure. The stability of aggregates in response to water was also found to be improved when constructed by earthworms.

Though not fully quantified yet, greenhouse gas emissions (carbon dioxide, nitrous oxide, methane) of earthworms, direct or mediated by their strong influence on soil microbial communities, likely contribute to global warming, especially since top-dwelling earthworms increase the speed of carbon cycles and have been spread by humans into many new geographies.

Threats

Nitrogenous fertilizers tend to create acidic conditions, which are fatal to the worms, and dead specimens are often found on the surface following the application of various pesticides, among which insecticides and fungicides are the most toxic. In Australia, changes in farming practices such as the application of superphosphates on pastures and a switch from pastoral farming to arable farming had a devastating effect on populations of the giant Gippsland earthworm Megascolides australis, leading to their classification as a protected species. Globally, certain earthworm populations have been devastated by deviation from organic production and the spraying of synthetic fertilizers and biocides, with at least three species now listed as extinct, but many more endangered.

Economic impact

Various worms are used in vermiculture, the practice of feeding organic waste to earthworms to transform it into vermicompost. These are usually Eisenia fetida (or its close relative Eisenia andrei) commonly known as the brandling worm, or tiger worm or red wiggler. They are distinct from soil-dwelling earthworms, living mainly in manure heaps. In the tropics, the African nightcrawler Eudrilus eugeniae and the Indian blue Perionyx excavatus are used.

Earthworms are sold all over the world; the market is sizable. Doug Collicutt states, "In 1980, 370 million worms were exported from Canada, with a Canadian export value of $13 million and an American retail value of $54 million."

Earthworms provide an excellent source of protein for fish, fowl, and pigs, but have also been used traditionally for human consumption. Noke is a culinary term used by the Māori of New Zealand to refer to earthworms, which they consider delicacies for their chiefs.