MNP Ecology Center

Earthworms phylum Annelida Clitellata Oligochaeta

There are >7000 species known from aquatic and terrestrial habitats, and a small number of species are known to inhabit marine sediments. Most species belong to about 20 families adapted for a terrestrial interstitial habitat. Their distribution is limited by absence of soil organic matter and litter on which they feed. They are absent or rare in arid or cold regions, for climatic as well as nutritional reasons. Their present geographical distribution seems to carry the mark of previous glaciation events, so that they probably disappeared from regions covered by Pleistocene ice sheets (Michaelsen, 1903). Their northward recoloniza-tion had not reached many regions of Canada when European colonization of North America began. Human travel and migrations in recent times have expanded the range of many species. These exotic species are called peregrine, because their dispersal was caused by human activity. Species that were already locally present are called endemic species. Some peregrine species have been effective at displacing endemic species, particularly in disturbed or agricultural regions. We will first consider the suborder Lumbricina and then briefly the suborder Enchytraeina.

For general reference and more details on aspects of morphology and ecology, the reader is directed to Edwards (1998), Edwards and Bohlen (1996), Lee (1985) and Grasse's encyclopaedia. The physiology of earthworms is treated further in Laverack (1963). Compared with the onychophorans, for our purpose and in general, the main differences are the elaboration of the circulation system with a capillary network, of nephridial excretion and of the central nervous system. These permit a larger body and more complex behaviour. The body consists of repeated segments, the somites, which are partially independent. There are more organs, and tissue differentiation is more extensive.

Lumbricina, or true earthworms

The cuticle of earthworms is thin and flexible, so that juveniles grow into the adult size without moults. As in previous taxa, it is secreted by the epidermis; however, it is not chitinous, but collagenous and only 1-4 ^m thick (Jamieson, 1981). The epidermis, as in other tissues of annelids, is elaborated, with more diverse differentiated cells and often additional layers of cells. The epidermis and cuticle are traversed on the dorsal side by numerous canals from the coelom to the exterior. These normally are closed but permit passage of water into and out of the body for osmoregulation. The coelomic space of each somite is lined by a sheet of cells that form a septum between somites. The septum isolates the coelomic space between somites. The coelum is filled with a serous solution derived from the blood and the digestive tract, as well as by various types of free and motile coelomocytes, which are phagocytic and play a role in immunity. Their role is important because of the potential for bacterial invasion through the coelomic pores and wounds.

The coelom and nephridia function together in osmoregulation. Earthworms can lose up to 70% of their water content through the coelomic canals and cuticle, with soil desiccation. Under such soil hypertonic conditions, cells and tissues also lose water, and internal fluid electrolyte balance is affected. This may be important in initiating anhydrobiosis and periods of dormancy. In more dilute solutions or wet soils, the electrolyte balance is maintained. Rehydration occurs through the cuticle and restores cellular functions. There is one pair of nephridia in each somite, which clears coelomic fluid of soluble by-products and nitrogenous waste. The nephridia help to remove excess electrolytes, soluble organic molecules and generally maintain the physiological solution of the coelom. The concentration of the excreted urine varies with the hydration state of tissue fluids. As water becomes limiting, the proportion of excreted ammonia decreases and that of urea increases. Urea also predominates in starved individuals of Lumbricus and, in Eisenia, urea is always the main excreted nitrogenous waste. There is therefore some variation between species adaptations. In some species adapted to arid soils, such as Pheratina posthuma, urine from the nephridia is excreted into the intestinal tract. This conserves water for the tissues by re-absorption through the intestine. The intestine efficiently removes most of the water and releases a dry excrement through the anus.

There is a true closed blood circulation system, which enhances gas exchange and distribution of nutrients from intestinal cells to body tissues. A dorsal blood vessel pumps blood anteriorly and through a capillary network which supplies the tissues. The blood flows posteriorly through the ventral vessel. There are blood pigments which bind oxygen reversibly and remove CO2. The pigments are varied in annelids but tend to be haemoglobin in Oligochaeta. This permits a larger body size, higher activity and aerobic respiration under low oxygen tensions to 3% O2. Some species that live in limnetic mud are anaero-tolerant and have a metabolism adapted to tolerate anaerobic respiration, for up to 2 days. They have increased vascularization and modifications of the glycolysis to lactic acid pathway. The musculature consists of an outer circular layer with several inner circular and longitudinal muscle layers. They also articulate small chitinous setae, or podial extensions. These extensions are retractable, and used for grasping soil during locomotion and for burrowing into soil. Locomotion is facilitated by secretion of mucus from epidermal cells, through cuticle pores. The mucus absorbs water and maintains a wet slippery surface between the body and the soil. As it solidifies in the soil, it provides a rigid support to tunnel walls. The role of this secretion is also important in soil structure because its stickiness binds particles together and contributes to soil aggregate stability. This secretion is responsible for half of the total nitrogen released from the body.

Locomotion and behaviour of earthworms are coordinated by an elaborate nervous system. It consists of a central nervous system coordinated by cerebral ganglia in the brain, and paired ganglia in somites. The somite ganglia are connected by the ventral nerve cord. There are no specialized extensions on the head segment, as an adaptation for burrowing. The eyes are limited to photosensitive cells scattered on the head. The cuticle is highly innervated with touch-sensitive cells. Annelid burrowing forms often have gravitaxis detection, although they are not known in Oligochaeta. However, they are still able to right themselves if they fall on their back. Oligochaeta are capable of escape behaviour and memory. Therefore, there is a limited capacity for learning. The anterior head and mouth are highly innervated with chemosensory cells, which participate in directional search for food, avoidance of unpalatable particles and avoidance of toxicity. Therefore, food selection and migrations away from polluted sites occur. Food selectivity is affected by the concentration of phenolic, alkaloid and other cell wall molecules in plant litter or in the soil. For instance, leaf tissue can be made more palatable by first washing out these components (Mangold, 1953; Edwards and Heath, 1963; Satchell, 1967). Chemical sensitivity is well known from agricultural fields, where earthworms are kept out by many pesticides, herbicides and other chemical applications. A list of sensitivity to chemicals is provided by Edwards (1998). Sensitivity to chemicals is exacerbated by increased soil moisture, as chemosensory irritation is enhanced.

Food is ingested by suction created by the musculature of the mouth and pharynx. In some species, part of the pharynx is extensible for grasping. The ingested particles are then coated with a viscous mucus secretion. Food reaches the intestine by peristalsis of the intestinal wall musculature. There are, in sequence, one or more pouches for food storage, the crop and a gizzard. However, the crop is absent in some species. The gizzard has areas of reinforced cuticle that help macerate the food. This process helps to mix together the cellular tissues with mineral soil particles ingested at the same time. Digestion begins in the crop and gizzard with secretion of enzymes such as amylases, proteases and a lipase. The pH varies along the length of the intestine, from a slightly acidic anterior to a slightly basic (pH 7-8) middle and posterior. The intestine of some species contains chitinase and cellulase activity, but it is unclear to what extent these are contributed by intestinal bacteria and ciliate symbionts which can be present. Digestion of cellulose and chitin is normally attributed to endosymbiont activity. There is a gland in the upper intestine, the organ of Marren with chloragocytes, which contributes to the removal of ingested calcium and other abundant cations. These are precipitated as calcite and other crystals by a locally increased acidity. The crystals are excreted with the undigested remains of digestion. It is an important function, because ingestion of clays and plant matter can increase mineral concentrations to pathogenic levels, if they are all absorbed. The gland also has functions similar to the vertebrate liver, in that it supports blood detoxification and stores glycogen. The chlorago-cytes also contribute to removal of heavy metals (Jamieson, 1981).

Reproduction is by reciprocal cross-fertilization of mating pairs, because individuals have both male and female organs - they are hermaphrodites. Many species can also reproduce by parthenogenesis. However, the offspring of parthenogenesis are often less virile and less fertile. Fertilized eggs are wrapped for protection in a cocoon secreted by the clitellum. The cocoon is remarkably resistant to decomposition. Depending on species, 1-30 eggs are laid, but this number varies with the age and with how fed the individuals are. The number of cocoons produced annually also varies between species, from five to 1000. Most species produce a few hundred, depending on temperature and food availability. In general, deep-burrowing species produce fewer cocoons, and near-surface species more of them. In some species, cocoon production is seasonal, as an adaptation to the climate. Development of the egg to adult requires several weeks or months, depending on abiotic variables. Since genetic polyploidy is common and varied (as in some plants), the consequences on speciation and in population genetic studies need to be considered.

Oligochaeta have an exceptional ability to regenerate from mechanical damage. This is demonstrated by two processes. The first is the ability to regenerate broken sections at the anterior or posterior. Cut off somites are regenerated by cell divisions of tissues from damaged somites. The coelomocytes are particularly active in this process, and many lost somites can be regenerated. The wound healing process requires hours to days, but recovery of lost somites may take weeks. During this time, mobility is limited and, especially if the anterior is lost, feeding is also impeded. The second is the ability to fragment into two or more sections, when the individuals reach a particular size. Lumbriculus can fragment spontaneously into as many as eight sections, which then regenerate at both ends to form complete, but smaller, individuals. This is a mechanism of asexual reproduction, reminiscent of clonal expansion in unicellular organisms. There are also two adaptations to unfavourable conditions. Some species have seasonal periods of dormancy, or diapause, during which they are inactive, and do not feed. This may last through cold or dry periods of the years. The individual remains inside a cyst which consists of hardened mucus, where they are still capable of fragmentation. Most species are also able to become temporarily quiescent, by anhydrobiosis, through unfavourable conditions. This reversible process involves both partial tissue dehydration and physiological quiescence. However, individuals in anhydrobiosis are not resistant to the same extremes of temperature and desiccation as Tardigrada or even nematodes.

Enchytraeidae, or potworms

Enchytraeids are morphologically similar to the Lumbricina, but several differences need to be highlighted. This single family of the suborder contains about 600 species, which have a broader geographic distribution than the Lumbricina (Didden, 1993). Individuals are much smaller, with most species being a few millimetres or less, though some can reach 5 cm. They do not form permanent burrows as do some earthworms, but travel through the soil organic layers. They can be found in subarctic regions as well as under snow and glacier ice. They are more abundant in forest soils and soils with a rich organic layer, and less abundant in pastures and agricultural fields. Their food preferences have been studied (Dosza-Farkes, 1982; Kasprzak, 1982; Toutain et al., 1982). They prefer macrodetritus or particulate organic matter that has been pre-digested by fungal and other saprotroph activity. Protists and mineral soil are ingested along with this litter. Interestingly, some species seem to have difficulty digesting cellulose, so that humus, hyphal and protist digestion may be more significant than plant tissue biomass ingested. Development of eggs in cocoons requires 2-4 months, varying with temperature and species. Parthenogenesis, self-fertilization and fragmentation are also common. Aspects of their ecology has been reviewed in van Vliet (2000) and Lagerloef et al. (1989).