The Structure of the Clitellum of Alma emini, Mich.

The Structure of the Clitellum of 

Alma emini, Mich. 

by 

A. J. Grove, M.A. (Cantab.), D.Sc. (Birm.), 

Lecturer in Zoology, East London College. 

With 4 Text-figures. 

CONTENTS. 

PAGE 

I N T R O D U C T I O N . . . . . . . . . . 2 2 3 

T H E C L I T E L L U M O F A L M A E M I N I . . . . . . 2 2 4 

T H E C L I T E L L U M O F D I A C H A E T A E X U L . . . . . . 2 2 7 

D I S C U S S I O N . . . . . . . . . . 2 3 0 

R E F E R E N C E S . . . . . . . . . . 2 3 3 

I N T R O D U C T I O N . 

THROUGH the kindness of Dr. J. Stephenson, I have been 

able to examine a specimen of Alma emini, Mich, (from 

Tanganyika), a Glossoscolecid belonging to the sub-family Microchaetinae. 

This worm possesses several remarkable features, 

particularly, an unusually long clitellum, the investigation of 

which seemed likely to throw some light upon the relation of the 

clitellum to the generative apertures in the evolution of the 

Oligochaeta, tentative suggestions regarding which were put 

forward by me as a result of the observations upon the reproductive 

processes of the Lumbricids Lumbricus and Eisenia 

(Grove, 1927, p. 471). 

In the Glossoscolecidae, the more usual position for the 

clitellum is in the region of the male pores, a condition which 

obtains in the sub-families Glossoscolecinae (except Opisthodrilus), 

Sparganophilinae and Hormogastrinae. In the Microchaetinae, 

however, while in the genera Microchaetus, 

Tritogenia, Glyphidrilus and Callidrilus the 

clitellum is in the region of the male pores, it lies well behind 

these apertures in the genera Kynotus, Drilocrius, and

224 A. J. GROVE 

Alma. This latter condition is also found in the Criodrilinae 

with its solitary genus Criodrilus. A distinctive feature of 

many of the species of these four genera is the unusual length of 

the clitellum (e.g. K. kelleri, twenty-six segments; D. 

biirgeri, thirty segments; A. pooliana, sixty-one segments; 

C. lacuum, thirty-two segments), but in the genus 

A1 m a, in addition to the often extreme length of the clitellum, 

the worms are characterized by the development, in connexion 

with the apertures of the vasa deferentia, of long processes to 

which is ascribed the function of the transference of the spermatozoa 

during coition. The position of the spermathecae, too, is 

remarkable; for, instead of occupying the more usual position 

anterior to the male pores, they are found either within or 

immediately in front of the clitellum. 

In the Lumbricidae, the investigations upon the reproductive 

processes showed that the clitellum participated in both coition 

and cocoon formation and that the posterior position of the 

clitellum had associated with it a conveying mechanism by 

which the spermatozoa during the former, and the eggs during 

the latter, were conveyed from the generative apertures to the 

clitellum. In A. e m i n i, however, the posterior position of the 

clitellum is combined with the development of a special mechanism 

in the form of penial processes for the conveyance of the 

spermatozoa during coition, and the clitellum consequently does 

not participate actively in the process, a condition which should 

result in corresponding differences in structure. 

THE CLITELLUM OF ALMA EMINI. 

The specimen of A. emini examined is intermediate between 

the two hitherto distinguished forms (Stephenson, 1928) the 

position of the clitellum agreeing almost exactly with that of the 

var. Aloysii-Sabaudiae, whilst the number and arrangement 

of the spermathecae conform more closely to that of 

the type. The clitellum is not clearly demarcated from the other 

segments of the body apart from a slight difference in colour. 

It extends from segment 55-100 (forty-six segments) and lies 

far behind the male pores, which are situated on penial processes 

arising from segments 18-20. The shape of the body behind the

CLITELLUM OF ALMA 225 

penial processes is markedly quadrilateral and this persists 

throughout the clitellar region. No papillae are visible on the 

clitellum. 

In a transverse section it is seen that, in spite of its lack of 

prominence externally, the clitellum is well developed, its glandular 

elements comprising more than one half of the thickness of 

the body wall. Its shape is roughly quadrilateral, but along the 

TEXT-FIG. 1. 

Semi-diagrammatic section through the clitellum of A. emini. 

circ mus, circular muscles; cl, the thickness of the clitellum; 

ens, central nervous system; longmus, longitudinal muscles. 

sides a groove is evident, accentuated doubtless by the preserving 

process, and the ventral surface is more convex than the 

dorsal. Duboscq (1902) describing the clitellum of Alma 

Zebangii, states: ' Dans les anneaux du clitellum, le tegument 

tout entier, dorsal et ventral, a subi la transformation glandulaire, 

laquelle accentue les sillons normaux au lieu de les effacer.' 

Much the same conditions were found in A. emini, for the 

distribution of the glandular elements is uniform throughout 

the circumference, and there is no obvious difference in the 

structure of the clitellum such as was found in Lumbricus 

and Eisenia, dividing it into regions. Although the material


had been merely preserved in alcohol without the use of special 

fixatives, it was possible to differentiate the various glandular 

A portion of the cliteilum ot A. emini (x 266). cu, cuticle; 

circ mus, circular muscles; / gr c, gland cells with fine granular 

contents ;lgrc, gland cells with large granular contents; long tmis, 

longitudinal muscles; mu c, mucin secreting cells. 

elements by the use of muci-haematin and picro-indigo-carmine, 

and also Mallory's triple-connective tissue stain (Grove 

and Cowley, 1927). In these preparations the same three types 

of unicellular glands were distinguished as were found in 

Lumbricus and Eisenia, viz., (a) mucin-secreting gland-

CLITELLUM OP ALMA 227 

cells, (b) gland-cells with large granular contents, and (c) glandcells 

with fine granular contents. The mucin gland-cells are 

fairly numerous, distributed rather irregularly, and somewhat 

elongated in shape, penetrating to some distance into the 

thickness of the clitellum. The large-granule cells are very 

numerous, uniformly distributed, and they too are elongated in 

shape extending still deeper into the thickness of the clitellum than 

the mucin gland-cells. The fine-granule gland-cells are arranged 

in groups separated from one another by sheets of connective 

tissue, the cells in each group forming columns in precisely the 

same way as was found in Lumbricus and Eisenia. 

Duboscq (1902) does not distinguish the mucin-secreting cells 

from the other superficial cells, but describes the large-granule 

cells, and the fine-granule cells he includes in a third layer as 

'une couche de longues cellules muqeuses qui forment les trois 

quarts de l'epaisseur du clitellum'. 

Apart from these characteristic constituents of the clitellum, 

no other glandular elements were distinguished such as were 

present in the Lumbricidae associated with the tubercula 

pubertatis or diverticula of the setal pores. 

In view of the rather specialized character of A. emini, it 

was thought desirable to compare the structure of its clitellum 

with that of a more typical Glossoscolecid, and, again through 

the kindness of Dr. Stephenson similar sections of the clitellum 

of Diachaeta exul, Steph., belonging to the Glossoscolecinae, 

were prepared. 

THE CLITELLUM OF DIACHAETA EXUL. 

The clitellum in this worm is only seven segments long, 

occupying segments 14-20. In the spirit specimens it is clearly 

marked in an external view by both prominence and colour, 

its smooth greyish-white surface contrasting with the darker 

colour of the other segments. The segments in the clitellum are 

clearly defined, and on the ventral surface of the eighteenth 

segment are found the male pores. These lie at the posterior 

ends of crescentic papilla-like structures which extend forwards 

across the anterior half of segment eighteen and invade the posterior 

border of the seventeenth segment. Apart from the setae,


the only other structures which are obvious externally are a 

series of pit-like depressions on the lateral sides, in line with the 

lateral setae and situated in the furrows between segments 

14/15 to 20/21, with indications of smaller depressions in furrows 

13/14 and 21/22. 

In a transverse section through the middle (segment eighteen) 

of the clitellum, the outline is roughly circular with no marked 

TEXT-FIG. 3. 

\---cL 

•pap 

-arc mus 

-Long mus 

Semi-diagrammatic section through the clitellum of Diachaeta exul. 

circ mus, circular muscles; cl, the thickness of the clitellum; 

ens, central nervous system; long mus, longitudinal muscles; 

pap, papilla. 

divisions into regions in accordance with the distribution of the 

glandular elements. The glandular portion comprises the 

greater part (3/4ths) of the thickness of the body-wall, and is 

uniform in thickness around the whole circumference, there being 

no appreciable thinning on the ventral surface. The same three 

types of unicellular glands are distinguishable as in Alma. The 

mucin-secreting glands are somewhat irregularly distributed and 

are relatively small in size, not penetrating deeply into the 

thickness of the clitellum. The large-granule containing cells 

too, although penetrating deeper than the mucin cells, are


relatively superficial. The fine-granule containing gland-cells 

have the same characteristic shape and distribution as in Alma 

except that the cells are much broader relatively to their length, 

and the narrow duct-like prolongations leading up to the surface 

are not so clearly defined. 

The crescentic papilla-like structures found in relation with 

TEXT-FIG. 4. 

A portion of the clitellum of D. oxul (x 266). circmus, circular 

muscles; cu, cuticle ;fgrc, gland cells with fine granular contents; 

I gr c, gland cells with large granular contents; long mus, longitudinal 

muscles ; mu c, mucin secreting cells. 

the apertures of the vasa def erentia contain none of the specialized 

clitellar glands. Scattered isolated mucin cells were found in 

preparations stained with muci-haematin and picro-indigocarmine, 

but with Ehrlich's haematoxylin the papilla appeared 

to be covered externally by an epidermis of short cells with welldefined 

nuclei, and internally, to consist of a stroma composed 

of irregularly arranged cells with scattered nuclei. In transverse 

section, each papilla is composed of two prominent lips 

with a deep furrow between, and is in connexion with the mass 

NO. 294 Q


of cells which penetrate the layers of muscle of the body-wall, 

projecting into the body cavity. The vas deferens passes through 

this collection of cells and opens into the base of the furrow. It 

will be seen also, that these structures do not invade the glandular 

portion of the clitellum, and, apart from them, no other 

glandular structures are present. 

The pit-like depressions that are so obvious on the external 

surface mark the apertures of the nephridia. 

DISCUSSION. 

It is evident that so far as its general glandular constitution 

is concerned, the clitellum of A. emini does not depart from 

that found in the more typical Glossoscolecid D. exul. In 

addition, the gland-cells present show a marked similarity in 

their constitution and arrangement to those which, in the 

Lumbricidae, have been shown to be concerned with cocoon 

secretion. In A. emini we have an example of an Oligochaete 

in which the development of special penial processes in connexion 

with the apertures of the vasa deferentia has removed from the 

clitellum the necessity of active participation in coition such as 

has been associated with its posterior position in other cases. 

The position of its spermathecae, opening as they do in the 

furrows between segments 52/53-84/85, suggests that the spermatozoa 

will in all probability be deposited on the clitellum, but 

the clitellum itself will play a more passive role than where it 

is concerned, as in Lumbricus and Eisenia, with the 

collecting of the spermatozoa around the apertures of the 

Spermathecae. (In this connexion it must be remembered that 

in other species of Alma the spermathecae may lie entirely 

in front of the clitellum—e.g. A. stuhlmanni, A. schultz 

ei, &c.—and consequently the clitellum will not be included in 

the region to which the penial processes would be applied, so 

that even in A. e m i n i it can be regarded as not participating 

as such in the process of coition.) The remaining outstanding 

feature is therefore its length. 

No description of the cocoon of A. emini appears to exist, 

but that of A. multisetosa has been described by Michaelsen 

(1915, p. 304): 'Die Kokons sind ungefahr 130-155 mm. lang


und in der Mitte 9-10 mm. dick, langspindelformig, an den 

Enden diinner werdend und schliesslich in sehr dunne, etwa 

10-15 mm. lange Endschlauche ausgezogen.' A. multisetosa 

is a large worm (Michaelsen, 1915, p. 280) more than 240 

mm. long and 8 mm. thick, the clitellum extending from 80-136 

segments (fifty-seven segments). Dr. Michaelsen has very kindly 

lent me one of the four cocoons from which his description was 

made. This had been opened and found to contain thirty-two 

embryos in a fairly advanced stage of development. The cocoon 

membrane had much the same appearance as that of the cocoons 

of Lumbricus and Eisenia. The age of the cocoon, as 

evidenced by the advanced development of the contained 

embryos, rendered it extremely unlikely that any remains of 

a cocoon slime-tube would be found, and careful examination 

failed to reveal anything which could be determined as a slimetube. 

Nevertheless, the presence of mucin secreting glands in 

the clitellum would provide the means for the production of this 

structure. 

The only other Glossoscolecid cocoons that I have been able 

to examine are those of Criodrilus lacuum in the collections 

of the British Museum (Natural History). In this worm 

the clitellum is also long (Michaelsen, 1900, gives it as more than 

thirty segments, and in a specimen examined, it appeared to 

extend from segment 16 to 47). The cocoon, too, is long, narrow, 

and spindle-shaped, with long-drawn-out prolongations at either 

end. These prolongations vary in different cocoons and it has been 

impossible to determine whether a slime-tube is present or not. 

It is a remarkable occurrence that in both of these worms, 

each of which is distinguished by the possession of an extremely 

long clitellum, the cocoon has this unusual elongated-spindle 

shape so unlike that of most Oligochaete cocoons. The obvious 

conclusion that may be drawn is that these two conditions are 

intimately associated. Michaelsen (1929) discussing the question 

of the extent of the clitellum in the Oligochaeta states that the 

length of the cocoon is determined by the size and number of 

worms which complete development, thus (p. 697): ' Schon bei 

den relativ kleinsten Kokons muss die Giirtellange die Dicke 

des Wurmes betrachtlich iibertreffen.. Hat der Kokon mehrere 

Q2


und relativ grossere Jungwurmer zu liefern, muss also sein 

Inhalt grosser sein, so kann er dies nur durch Zunahme seiner 

Ltinge erreichen, denn die Kokondicke, entsprechend der Dicke 

des Wurmes, ist beschrankt.' 

As already noted above, the long cocoon of A. multisetosa 

contained thirty-two embryos, but there is no evidence as to 

what proportion of the original number of eggs laid this represents 

or the number which will eventually reach maturity. 

Orley (1887) records that in Criodrilus the number of eggs 

varies from 8-20, but that usually only about one-third of the 

number develop, the largest number of embryos found being 

eight and the smallest two. 

It is possible, though its significance is not easy to see, that 

the spindle-shaped cocoon produced by these two worms may 

have some connexion with their particular habitat, for in both 

cases the cocoons are produced at the time the muddy swamps in 

which they live are drying up. 

So far as A. e m i n i is concerned, therefore, all that can be 

said with certainty is that the extreme length of the clitellum is 

merely a concomitant of the unusual length of the cocoon, and 

has no relation to the other reproductive processes. It is of 

interest that the glandular constituents of the clitellum support 

the view that it is concerned with cocoon formation only, as would 

be expected from the development of the special penial processes, 

but this interest is enhanced by conditions found in D. e x u 1, 

for in that worm also the glandular constituents of the clitellum 

proper are solely those which in the Lumbricids are concerned 

with cocoon formation. This, in view of the close association of 

the male apertures with the clitellum is rather unexpected and 

further work on the process of coition in the Glossoscolecids, 

which, however, would only be of value if carried out with living 

material, is necessary before any definite statement could be 

made. It is possible that the secretion of the glands in connexion 

with the crescentic papillae associated with the apertures of the 

vasa deferentia may suffice to effect any attachment necessary 

during the transference of the spermatozoa, or that the papillae 

themselves may operate in the same way as described by Bahl 

(1927) in Eutyphoeus.


Many points have come to light during the examination of 

sections prepared during this investigation which suggest the 

possibility of the existence of a carrying mechanism for the 

backward conveyance of the eggs into the cocoon prior to deposition 

; and the presence of the spermathecae in the clitellar region 

offers a simple explanation of the entry of the spermatozoa. But 

the absence of opportunity for observing these processes in the 

living worm precludes the possibility of elaborating these further 

at present. 

EEFERENCBS. 

Bahl, K. N. (1927).—"On the Reproductive Processes of Earthworms: 

Pt. 1. The Process of Copulation and Exchange of Sperms in Eutyphoeus 

waltoni, Mich.", 'Quart. Journ. Micr. Sci.', vol. lxxi, pp. 479—502. 

Duboscq, 0. (1902).—"Alma Zebangii, n.sp., et les Alminae Oligochaetes 

de la Famille des Glossoscolecidae, Mich.", 'Arch, de Zool. exp. et gen.', 

3 ser., vol. x, Notes et Revues, pp. xcvii-cvi. 

Grove, A. J. (1927).—"The Passage of the Spermatozoa into the cocoon in 

the Brandling Worm (Eisenia foetida, Sav.)", ' Quart. Journ. Micr. Sci.', 

vol. lxxi, pp. 465-77. 

Grove, A. J. and Cowley, L. F. (1927).—"The Relation of the Glandular 

Elements of the CliteUum of the Brandling Worm (Eisenia foetida, Sav.) 

to the Secretion of the Cocoon", ibid., vol. lxxi, pp. 31-45. 

Michaelsen, W. (1900).—"Oligochaeta", 'Das Tierreich', Bd. X. Berlin. 

(1915).—"ZentralafrikanischeOligochaten", 'Ergebnisse der Zweiten 

DeutschenZentral-Afrika-Expedition 1910-1911', Bd. 1, pp. 185-317. 

(1929).—"Zur Stammesgeschichte der Oligochaten", 'Zeitschr. wiss. 

Zool.', Bd. 134, pp. 693-716. 

Orley, L. (1887).—"Observations on Criodrilua lacuum", 'Quart. Journ. 

Micr. Sci.', vol. xxvii, pp. 551-60. 

Stephenson, J. (1928).—"Oligochaeta from Lake Tanganyika (Dr. C. 

Christy's Expedition, 1926)", 'Ann. and Mag. Nat. Hist.', ser. 10, vol. 1, 

pp. 1-17.

The Structure of the Clitellum of Alma emini, Mich.

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