Criodrilus, Hoffmeister, 1845

Rota, Emilia, 2022, REVIEW How the discovery of oligochaete regeneration during the Enlightenment was pivotal to the advancement of annelid research, Zoological Journal of the Linnean Society 196 (1), pp. 1-24 : 19-21

CRIODRILUS , THE BOAT-WORM

Criodrilus lacuum Hoffmeister, 1845 is well known today as a limicolous earthworm, with a long quadrangular body comprising 200–450 segments and dorsally grooved from the midregion, inhabiting the muddy banks and bottom of rivers, ditches, ponds, swamps and even rice paddy systems. Its anatomy is similar to that of common earthworms, except for the lack of dorsal pores, gizzard and spermathecae. Spallanzani provided an exhaustive description of it on 12 June 1766, when its odd floating-tail posture first attracted his attention in the ditches at La Villetta, near Modena, suggesting the name of boat-worm ( Spallanzani, 2003: 212–214), or the ‘Modena worms’. A more complete morphological account was given in the Prodromo:

Its size towards the head is equal to one of the largest goose quills, and its length about a span. The largest ones indeed may reach to the middle of the arm, especially when stretched. The colour of their back is dark, but grows lighter towards the tail; the belly is of a pale flesh hue. [It lives] in sweet, shallow, and clear waters, either stagnating or flowing gently. ( Spallanzani, 1769: 19–20)

The boat-worm showed a great regenerative power:

The three earthworms [of the ditch of Modena], which the first of this month I mutilated for the 12 th time, and which is more than a year that I have [September 1766 – September 1767], have reproduced a lot of tail. ( Spallanzani, 2003: 548)

It was also prone to self-amputation, and frequently (95%) on collection showed evidence of one or multiple episodes of tail regeneration.

In some of the worms extracted from the ditch, I discovered two reproductions that occurred at different times, as shown so well by their different colour. The head together with a portion of the body had its natural brown; the other portion closer to the tail had a lighter brown colour; and the third one which hung to the tail was reddish white. I also found a worm in which one could clearly distinguish three successive reproductions. (letter to Bonnet dated 21 September 1766, in Biagi, 1958: 109, translated by Tsonis & Fox, 2009, here partly revised)

The broken worms never failed to become boat shaped at their posterior end.

I have learned that though I have cut a slice of the tail, the end of the stump did not stop appearing on the surface of water and become boat-shaped as usual. I had the idea of successively shortening the length of the worm by taking off new slices at different steps. With this experiment I had two objectives: the first was to know if the fresh water worm would always use the remaining part of the body to make a boat-shaped structure; the second was to know if the reproduction would show in different sites of the length of the sectioned animal. Both were proven wonderfully. Regeneration and the boat shape did not stop to appear. The length of the worm so sectioned again and again had been reduced to one thumb and a quarter. I found I had the right to draw that conclusion: that the strength of regeneration is present almost in the whole length of the worm. (letter to Bonnet, dated 21 September 1766, in Biagi, 1958: 110–111, translated by Tsonis & Fox, 2009, partly revised)

Regeneration proceeded much faster and more easily than in terrestrial species, also at the front end and in the winter season.

These worms reform their heads also when they are cut posteriorly; and the reproduction of the head is easier in these, than in those inhabiting the earth. These reproduce even in winter; even the head. I have had twelve consecutive reproductions, and nevertheless they have not diminished much in size. ( Spallanzani, 2003: 550)

The anus gradually reformed as a subterminal, dorsal, elliptic opening ( Fig. 7 ).

The shape of the anus stretches out, the cone surrounding it grows, particularly at the base, where it is implanted in the stump. The extremity of the anus towards the head shows no sign of reproduction but is marked by a small dorsal red line having the same direction as the artery of the stump. Blood circulation appears the next day and it can be seen that the blood in that vessel moves rhythmically as in the gross artery, into which it flows. The cone gradually grows and becomes longer.The edges of the anus acquire more redness, and after one day and a half, blood is seen flowing in them, and continuing in the reproduced vessel. So, it is certain the gross artery draws its origin from the two branches united in an oval structure corresponding to the edges of the anus. Then the cone is finally seen being composed by rings; but these rings are so tightly close to each other that it is impossible to catch the exact number of them. ( Spallanzani, 2003: 550)

The behaviour of the boat-worm was different in cold weather:

Concerning my Modena worms, during the winter, although some have raised their tails a bit out of the mud, yet none has put it out of the water making the boat. One day at La Villetta, exploring the ditch where they live in abundance, I found it frozen and covered in snow. So, I noted that they do not necessarily live in warm springs like many other insects, and they do not need to keep the tails out of the water to survive. I also noticed that once they get out of the mud they retreat slowly, while in the summer they do it very quickly. ( Spallanzani, 2003: 359)

Although all the above is typical of Criodrilus , the boat-worm remained unrecognized and mysterious until 1976, when the species was identified by Andreina Paoletti Di Chiara (see Belloni, 1976). The long failure to identify the boat-worm can be explained by the seasonally changing respiratory posture and by the very rough freehand sketches published by Spallanzani. Formally first described from Tegelsee, near Berlin, Germany ( Hoffmeister, 1845), Criodrilus lacuum was recorded a second time under this name only 30 years later, from rice fields along the Po River ( Panceri, 1875) in Italy, and then from the Danube Basin in Austria ( Hatschek, 1876) and Hungary (Örley, 1885). In 1886, Rosa found it again in Italy, in the Venetian area near Treviso and in marshes near Turin, and in 1920 at a locality close to Spallanzani’s site: Saliceta Panaro, in the periphery of Modena. Rosa (1888) was the first to observe and effectively describe the respiratory behaviour of Criodrilus , probably because the thermal regime of water bodies in Italy induces the floating-tail posture more frequently.

Many early accounts of Criodrilus mentioned the conspicuous horn-like spermatophores and the long (≤ 5 cm) spindle-shaped cocoons, fixed to surrounding plants; but the worms never showed any trace of a clitellum. Benham (1887), based on histological sections, first located this organ, over segments XVI– L. Such a long clitellum, subject to seasonal regression and producing elongate cocoons, is not unique to Criodrilus , nor is the floating-tail respiratory behaviour unique among aquatic megadriles [e.g. see remarks on the lumbricids Allolobophora dubiosa (Örley, 1880) and Helodrilus mozsaryorum (Zicsi, 1974) in Csuzdi & Zicsi (2003: 102 and 174); and the biwadrilid Biwadrilus bathybates (Stephenson, 1917) in Blakemore (2008)]. Perhaps the most astonishing similarities are found among Glyphidrilus species (family Almidae ) inhabiting rivers in Thailand: their clitellum can cover ≤ 50 segments, the posterior part of the body is dorsally grooved to form a U-shaped channel allowing water circulation down the burrow, and the expanded and flattened tail tip protrudes over the substrate or on the water surface ( Chanabun et al., 2013: figs 1B, 23B).

The extraordinary power of regeneration of Criodrilus lacuum had been noticed since its formal taxonomic description ( Hoffmeister, 1845) and later thorough investigation by various authors (e.g. Collin, 1888; Janda, 1912, 1926; Tirala, 1913). Janda (1912) showed that Criodrilus can regenerate the same or almost the same number of segments after the loss of the entire genital region and even larger parts of the body; after removal of 40 front segments, the worm was still capable of anterior regeneration.

Figures

Figure 7. Spallanzani’s observations on his ‘lombrico a batello’, or ‘boat-worm’ (Criodrilus lacuum Hoffmeister, 1845). A, B, respiratory posture, with the head buried in the mud and the tail floating on the water surface. C, close-up of the richly vascular tail. D, E, regeneration of the caudal region and reforming of the anus. A, C–E, reproduced from Spallanzani (2003). B, reproduced from Biagi (1958: 108).