Main Content
< Top page

The World of Protozoa, Rotifera, Nematoda and Oligochaeta

Eisenia

Eisenia Malm, 1877 (ref. ID; 3692, 6916) or Malm, 1877 emm. Michaelsen, 1900 (ref. ID; 1257)

Family Lumbricidae (ref. ID; 1928, 6033)

Family Lumbricidae: Subfamily Eiseninae Omodeo, 1956 (ref. ID; 1257)

ref. ID; 1923

Clitellum beginning on segments 18 to 23 and extending over 4 to 6 segments; male pores on segment 12, 13, or 15, conspicuous; gizzard limited to segment 17; first dorsal pores on segments 4/5. (ref. ID; 1923)

ref. ID; 6916

The individuals belonging to this genus display a reddish colour, epilobous prostomium, closely paired setae, first dorsal pore around 4/5, calciferous gland without pouches in 10, four pairs of vesicles in 9-12, two pairs of spermathecae in 9/10, 10/11, nephropores inconspicuous and alternating irregularly and nephridial bladders sausage-shaped (Bouche 1972; Gates 1975, 1978; Fender 1985; Sims and Gerard 1999; Csuzdi and Zicsi 2003). There seems to be some heterogeneity in the somatic characters in the species included in this genus when compared to the type species, Eisenia fetida (Savigny, 1826), according to Gates (1975) and Csuzdi and Zicsi (2003). Up to four species are described in the Frence fauna: E. fetida fetida (Savigny, 1826), E. fetida andrei Bouche, 1972, E. submontana (Vejdovsky, 1875) (a synonym of E. lucens; see Blakemore 2007), E. eiseni (Levinsen, 1884) and E. parva (Eisen, 1884), whereas for British fauna Sims and Gerard (1999) provide a different species list: E. fetida, E. andrei, E. hortensis Michaelsen (1900) and E. veneta (Rosa, 1886). Besides the disagreement in the taxonomical nomenclature of L./E./Ad. eiseni, there are two addition important discrepancies between the French and British classifications. Sims and Gerard (1999) give E. andrei species level status and include E. hortensis and E. veneta as Eisenia species instead of within the Dendrobaena genus (sensu Bouche 1972; Csuzdi and Zicsi 2003; Blakemore 2007). Furthermore, Bouche (1972) regards them as subspecies, i.e. D. veneta veneta (Rosa, 1886) and D. veneta hortensis (Michaelsen, 1889) (misspelt as venata). It is important to notice here that several of Bouche's taxa has been considered invalid and corrected according to the priority principles of taxonomy (Blakemore 2007). This has led some authors to claim an urgent need for a revision of the genus Eisenia (Csuzdi and Zicsi 2003). Our trees clearly indicate that this genus is not monophyletic, confirming this need. The two compost worms (E. fetida and E. andrei) are morphologically very similar with the exception of their pigmentation (Sims and Gerard 1999) and Bouche (1972) considered them as subspecies due to the lack of hybrids in nature, Jaenike (1982) provided the first genetic evidence of the existence of separate lineages, which was followed by others concluding that they are indeed different species (Henry 1999; McElroy and Diehl 2001, Perez-Losada et al. 2005). In addition, they seem to the reproductively isolated (Elvira et al. 1996; Dominguez et al. 2005) which supports their consideration as two different identities. However, the validity of E. andrei has been recently questioned by Cech (2005) who re-analysed the material assigned as E. andrei in the GenBank by Erseus and Kallersjo (2004) and concluded that it has probably been mistaken with Dendrodrilus subrubicundus. Consequently, it is not recognised as a valid taxon by Blakemore (2007, 2008) due to the arbitrary of its specific status between authors. In our case, the morphological and anatomical difference used to distinguish between E. fetida and E, andrei is the result of many years spent studying a high number of specimens from a wide variety of biogeographical regions of the Iberian Peninsula (Alvarez 1966, 1967, 1971, 1972, 1973; Diaz-Cosin et al. 1980, 1986, 1992; Calvin et al. 1985; Mato 1986; Mascato 1986; Marino et al. 1986, 1987; Trigo et al. 1988, 1990; Briones et al. 1991, 1992, 1994; Souto 1992, 1996; Souto and Mascato 1993; Sanchez et al. 1998, 1999; Monroy 1999; Monroy et al. 2003). Furthermore, they appear to be clearly sister taxa in our trees (96% BS in both trees), with an amount of divergence similar to the amount observed in the same tree between different species. Similar results were obtained by Pop et al. (2005) for populations collected in Spain and Romania, although with lower BS support (41% and 67% for 16S and COI, respectively). However, more research is needed to clarify the taxonomic status of these two species (Cech 2005) and to test the validity of the synonymic names for E. fetida listed in the literature (e.g. Csuzdi and Zicsi 2003; Blakemore 2007, 2008) as well as to determine the variability of this latter species as it is possible that several "varieties' are involved (Perez-Losada et al. 2005). Regarding whether E. hortensis and E. veneta should be included either within Eisenia or Dendrobaena, the distinction between these two genera has always been problematic because it is classically based on somatic characters. Indeed close relationships have been suggested between these two genera based on their musculature (Kvavadze 1985). However, the genus Eisenia contains species with pinnate, intermediate or fasciculated musculature (Csuzdi and Zicsi 2003). The shape of the nephridial bladder has also been considered to be particularly important (sausage and ocarina-shaped, respectively) and, following these criterion, these two species should be included in Eisenia (see also Fender 1985). Another diagnostic aspect which has been of great relevance in the classification of the Lumbricidae is the number of seminal vesicles. The primitive condition was the octovesiculate battery (Eisenia and others) which evolved to a sexvesiculate one in the 'Dendrobaena stage' (Gates 1974). Unfortunately these organs appear to undergo rudimentation and deletion in the different populations analysed, and this possibly explains the discrepancies observed in the descriptions of these two species. Thus, E. hortensis has been described as having three pairs after loss of the one in segment 10 (Bouche 1972; Gates 1978; Csuzdi and Zicsi 2003) or four pairs with either or both of the anterior pairs failing of develop (Sims and Gerard 1999). Three pairs are also present in E. veneta according to Bouche (1972) but four according to Sims and Gerard (1999) and Csuzdi and Zicsi (2003). Therefore, in order to clarify their anatomical description and taxonomical position, and to avoid future confusion, we performed detailed anatomical study of specimens belonging to both species and collected from two English sites. The results show that they are both very different from one another in pigmentation, size, setal distance, number of seminal vesicles and shape of the typhlosole, but show important similarities such as the position of the clitellum and tubercula pubertatis, their calciferous gland lacking pouches in 10, the number and location of the spermathecae, the shape of the nephridial bladder, the same chromosome number (36) and amphimictic reproduction. Their geographical distribution might be associated with human activities (Csuzdi and Pavlicek 1999) and accordingly, our phylogenetic trees show that both species are indeed sister taxa (84% BS for 16S), but placed far from the two compost worms. E. fetida and E. andrei, suggesting an independent origin. The fact that both species have a higher basic chromosome number (n=18) than the other two Eisenia species investigated here (n=11), could support their inclusion in the Dendrobaena genus (sensu Bouche 1972; Csuzdi and Zicsi 2003). However, convergence processes in the Oligochaeta is a common phenomena (Stephenson 1930) and have resulted in the existence of several chromosome number within the same genus (Casellato 1987). In order to maintain the nomenclature stability we, therefore, propose to retain them in Dendrobaena until further analyses are carried out on test type specimens (e.g. paratypes of topotypic material). (ref. ID; 6916)
  1. Eisenia altaica (Perel) (ref. ID; 7651)
  2. Eisenia andrei Bouche, 1972 (ref. ID; 6036) reported year? (ref. ID; 2170) reported author and year? (ref. ID; 6033)
  3. Eisenia carolinensis Michaelsen (ref. ID; 7651)
  4. Eisenia eiseni Levinsen, 1884 (ref. ID; 6036, 6916) reported author and year? (ref. ID; 6033)
  5. Eisenia fetida (Savigny, 1826) (ref. ID; 6036, 6916, 6947) reported author and year? (ref. ID; 6033)
  6. Eisenia fetida andrei Bouche, 1972 (ref. ID; 6916)
  7. Eisenia fetida fetida (Savigny, 1826) (ref. ID; 6916)
  8. Eisenia foetida (Savigny, 1826) (ref. ID; 1257, 3692) reported year? (ref. ID; 1928, 7651)
  9. Eisenia gordejeffi (Michaelsen) (ref. ID; 7651)
  10. Eisenia hortensis Michaelsen, 1900 (ref. ID; 6916)
  11. Eisenia japonica Michaelsen, 1891 (ref. ID; 6177)
  12. Eisenia kucenkoi (Michaelsen) (ref. ID; 7651)
  13. Eisenia lagodechiensis (Michaelsen) (ref. ID; 7651)
  14. Eisenia lonbergi Michaelsen (ref. ID; 7651)
  15. Eisenia lucens (ref. ID; 6033)
    See; Eisenia submontana (ref. ID; 6916)
  16. Eisenia macrura (Friend) (ref. ID; 1928)
  17. Eisenia malevici Perel (ref. ID; 7651)
  18. Eisenia moderata Cekanovskaja, 1959 (ref. ID; 3692)
  19. Eisenia nordenskioldi (Eisen, 1879) (ref. ID; 3692, 6889) reported year? (ref. ID; 7651, 7764)
  20. Eisenia parva (Eisen, 1884) (ref. ID; 6916) reported author and year? (ref. ID; 6033)
  21. Eisenia perelae Kvav. (ref. ID; 7651)
  22. Eisenia rosea (Savigny, 1826) (ref. ID; 3692) reported year? (ref. ID; 1257, 1928, 7651)
    Syn; Allolobophora rosa f. typica (Savigny, 1826)
  23. Eisenia salairica Perel (ref. ID; 7651)
  24. Eisenia submontana (Vejdovsky, 1875) (ref. ID; 6916) reported year? (ref. ID; 7651)
    Syn; Eisenia lucens (ref. ID; 6916)
  25. Eisenia tetraedra (Savigny, 1826) (ref. ID; 1923) reported year? (ref. ID; 1928)
  26. Eisenia tetraedra var. tetragonura (Friend) (ref. ID; 1928)
  27. Eisenia uralensis Mal. (ref. ID; 7651)
  28. Eisenia veneta (Rosa, 1886) (ref. ID; 6916) reported year? (ref. ID; 1928)
  29. Eisenia veneta var. hibernica (ref. ID; 1928)
  30. Eisenia veneta var. tepidaria Friend (ref. ID; 1928)
  31. Eisenia veneta var. zebra Michaelsen (ref. ID; 1928)

Eisenia fetida (Savigny, 1826) (ref. ID; 6036, 6916, 6947) reported author and year? (ref. ID; 6033)

Remarks

When encountered under intensive cultivation this species appears uniformly pigmented. Sims (1983) states that the uniformly pigmented "forms" seem to be derived from the "striped forms". The two forms, however, differ to such an extent that many researchers believe them to be phenotypic variants. Avel (1937) and Jaenike (1982) regard the uniformly pigmented "form" as a separate species. Sims (1983) pointed out that, despite presenting evidence of the apparent biological isolation of these two "forms", Andre (1963) made them conspecific by naming the uniformly pigmented "form" "var. unicolor" and the striped "form" "var. typica". Bouche (1972) gave the uniformly pigmented worm the new subspecific name Eisenia fetida andrei. Apart from the difference in pigmentation the two forms cannot be distinguished. Both "forms" have a mean length of 60-120 mm, a diameter of 3-6 mm and a segment number varying between 80 and 120. The saddle-shaped clitellum covers 6-8 segments. The tubercula pubertates stretch along the ventral border of the clitellum over three segments. The cocoons are 2.4-5.2 mm long with a diameter of 2.3-4.4 mm (Sims and Gerard 1985). It is difficult to reliably assign these forms to separate taxa since taxonomy is ultimately based on preserved type-specimens in which the distinguishing characters can be observed, but pigments in earthworms are not preserved (Sims 1983). Sheppard (1988) referred to Andre (1963) and stated that E. fetida "comprises not one but two species which can be distinguished by pigmentation". He considered the banded worms to be E. fetida (the common "brandling" or "tiger" worms) while E. andrei is uniformly pigmented dorsally (commonly known as the "red" worm). Sheppard (1988) found that while both forms performed similarly in terms of cocoons produced per unit time and cocoon viability, there was a significant difference in the numbers of progeny per cocoon produced by the two forms. Sheppard (1988) is convinced that this difference is further evidence for the specific status of the two forms, since it demonstrates "ecological distinctions" between them. Roch et al. (1980) and Valembois et al. (1982) showed that the two "forms" differed biochemically. Jeanike (1982) used electrophoresis to show that at least three loci of both shared no common allelles, indicating reproductive isolation but not excluding hybridization. The genetic isolation may also be correlated with physiological, ecological and behavioral differences, making it important to distinguish between the two 'forms". (ref. ID; 6947)

Eisenia nordenskioldi (Eisen, 1879) (ref. ID; 3692, 6889) reported year? (ref. ID; 7651, 7764)

Descriptions

Three forms of this species are conventionally distinguished: The existence of several morphological forms of this species (some of which are sympatric) and its adaptive flexibility in varied ecological conditions drew attention to the genetic basis of these phenomena. As it turned out, this species has more than one polyploid form: the sympatric amphimictic diploid (2x = 24) E. nordenskioldi f. pallida and the amphimictic dodecaploid (12x = 144) E. nordenskioldi f. typica were found in the environs of Novosibirska (Grafodatsky et al. 1982); tetra (4x = 48) and hexaploid (6x = 72) E. nordenskioldi f. typica were found on the southern slope of the Tarbagatai chain (eastern Kazakhstan) and in the Tellerman forest near Voronezh, respectively; and the parthenogenetic decaploid race E. nordenskioldi f. acystis (10x = 110-115) was found in the Talasskii Alatau mountains (Perel and Grafodatsky 1983). According to Bulatova et al., (1987), the cited chromosome number of the diploid E. nordenskioldi f. pallida, was not accurately determined, 2x being equal to 36 (not 24). Therefore, dodecaploids should be treated as octoploids (8x = 144), and decaploids should be treated as septaploids (7x = 110-115), and hexaploids should be treated as tetraploids (4x = 72). Such a correction of ploidy degree was made by Omodeo (1962) in respect of E. spelea, when the karyotype of sibling species E. submontana was resolved (6x17 = 102). The rest of the polyploid strains should be studied again, since individual metaphase plates were used to define them, and the method of isolating them from the clitellum epithelial cells was, in fact, imperfect. As a result of our research, we discovered that amphimictic octoploids (8x = 144) are the most widespread of all the E. nordenskioldi races. They were found in sandy soils of a pine forest (Prioksky-Terrasnyi Biosphere Reserve, Moscow region), in tundra (Taimyr peninsula) (Bulatova et al. 1984), and in the environs of Magadan (Viktorov 1988). An amphimictic hexaploid (6x = 102) E. nordenskioldi f. typica was detected in the unmown steppe stretches in the Central-Chernozem Biosphere Reserve (Kurk region) (Viktorov 1988). An amphimictic tetraploid (4x = 72) E. nordenskioldi f. typica was found in the Dzanybek biological station (Kazakhstan), where it had been introduced in the early 1960s, its original habitat being an oak forest near the Eruslan River (Saratov region) (Bulatova et al. 1984). Hence, the extreme northern, north-eastern, western, south-western and southern parts of the E. nordenskioldi range are populated by its polyploid (4n, 6n, 8n) amphimictic races. In the case of E. nordenskioldi, the extreme northern races (8n) are amphimictic, and the southern races (7n) are parthenogenetic. Thus we come across the "inverted geographical parthenogenesis", which in its pure form suggest that parthenogenetic forms tend to occupy the northern parts of a species range (Vandel 1928). Three main ecological groups of earthworms are conventionally recognised: epigees, endogees and aneciques. These forms are fully represented by E. nordenskioldi: E. nordenskioldi diploid f. pallida is an endogee; tetra-, hexa- and octoploid races of E. nordenskioldi f. typica are epigees; and the sourth Siberian octoploid race which makes deep burrows is an anecique (the only one in the genus Eisenia). E. nordenskioldi apart, it should be emphasized that, while diploid races of polyploid series tend to inhabit soil mineral horizons, polyploid races of corresponding species live in litter or topsoil. Among other things, this tendency ensures niche partitioning of the di- and polyploid earthworm populations in cases of sympatric existence. In south Siberia, the sympatry of two E. nordenskioldi races is noted: diploid endogees E. nordenskioldi f. pallida and octoploid aneciques E. nordenskioldi f. typica. The observed pattern of the distribution of E. nordenskioldi suggests that polyploids are ecologically more successful than diploids. Owing to characteristics such as their "well-buffered" genotypes through number duplications, polyploids may withstand dramatic environmental fluctuations, which trend increase towards the edges of the area. The same characteristics make polyploids successful colonists. Some of them tend to "adapt themselves genetically" to the environment. (ref. ID; 6889)

Eisenia tetraedra (Savigny, 1826) (ref. ID; 1923) reported year? (ref. ID; 1928)

Descriptions

This species is widely distributed. (ref. ID; 1923)

Eisenia veneta var. zebra Michaelsen (ref. ID; 1928)

Descriptions

They are large, handsome worms, 120 mm long, and 8 mm broad. The number of segments is 150. Each segment has a dark purple band of pigment, alternating with a clear intersegmental area. The bands are more diffused and slightly broader than in the var. zebra. In the first 8 segments the pigment-rings are complete. They gradually go paler till about the 13th segment, where they terminate laterally just below the dorsal pair of setae. Behind this region the ventral surface is unpigmented. The colour is much paler in the dorsal region of segments 9 and 10, near the spermathecal pores. The first dorsal pore is between the 5th and 6th segment. The distances between the setae agree closely with those of the var. zebra. The setae on the 9th segment are seated on papillae. The girdle occupies segments 1/2 26 - 1/2 33; and the tubercula are on segments 1/2 29 - 1/2 32, agreeing in these points roughly with the var. zebra, and differing from the type form. Numerous colour varieties of the species are found, but Michaelsen thinks it is doubtful whether they are true varieties. The occurrence of closely similar forms at the extreme east and west of the area of distribution of the species is very interesting. The resemblance is probably due to parallel and independent variation, and not to a close genetic connection. (ref. ID; 1928)