Research Article
Research Article
The second species of the endemic Malagasy earthworm genus Howascolex Michaelsen, 1901; Howascolex farafangana sp. n. (Clitellata, Megadrili)
expand article infoCsaba Csuzdi, Malalatiana Razafindrakoto§, Yong Hong|
‡ Eszterházy Károly University, Eger, Hungary
§ University of Antananarivo, Antananarivo, Madagascar
| Chonbuk National University, Jeonju, Korea, South
Open Access


A recent survey of earthworms carried out in South East Madagascar resulted in collecting two species belonging to the endemic Malagasy earthworm genus Howascolex Michaelsen, 1901. One of the species proved to be identical to the generotype Howascolex madagascariensis Michaelsen, 1901. The other species Howascolex farafangana sp. n. represents the second species of the genus. The genus Howascolex was originally classified in the subfamily Octochaetinae Michaelsen, 1900. However, its close morphological similarity with the Malagasy acanthodriline species implies a homoplasious origin of the meroic excretory system of Howascolex and its inclusion in the family Acanthodrilidae Claus, 1880.


Oligochaeta , Octochaetidae , Acanthodrilidae , holonephridia, meronephridia, phylogeny


The genus Howascolex was described by Michaelsen (1901) for his peculiar species H. madagascariensis Michaelsen, 1901 found in a cave near Andrahomana, South Madagascar. This new species possessed a very characteristic excretory system composed of praeclitellar holonephridia accompanied by 4–6 meronephridia from the middle of the body. Because of the presence of meronephridia, the new genus was placed into the meroic subfamily Octochaetinae Michaelsen, 1900. Another characteristic feature of H. madagascariensis was the large intramural calciferous glands in 16.

Michaelsen (1922) added 3 more species to the genus; bidens, corethrurus, and merkaraensis found in Southern India. Although, these new species shared the characteristic intramural calciferous glands in 16 with H. madagascariensis they differed from the Malagasy type in the structure of the nephridial system being purely meroic with caudal megameronephridia found in many other Indian octochaetids (e.g. Eutyphoeus Michaelsen, 1900, Eudichogaster Michaelsen, 1902).

The genus Howascolex was revised and redefined by Pickford (1937) to include several meroic species from Central and South America like Wegeneriella beauforti Michaelsen, 1933, Eodrilus irpex Michelsen, 1911, Eodrilus eiseni Michaelsen, 1911 and Wegeneriella michaelseni Černosvitov, 1934. Černosvitov (1939) did not agree with moving the South American Wegeneriella michaelseni and Wegeneriella beauforti into the Malagasy genus Howascolex and on the basis of presence of extramural calciferous sacs in 14–15 proposed a new genus Wegeneriona to accommodate them.

Graff (1957) describing several Salvadorian meroic earthworm species erected a new subgenus Howascolex (Graceevelynia) for the Neotropical species differing from the nominal subgenus by the more anterior calciferous glands (in the region of 8–13 instead of 16). This placement was later refuted by Gates (1962) because all the Central and South American species relegated previously to Howascolex by Pickford (1937) and (Graff 1957) are purely meroic and lack holoic body part. Therefore, Gates (1962) moved all these species to Ramiellona Michaelsen, 1935.

Julka (1988) revising the octochaetid earthworm fauna of India recognized, that the three Howascolex species described by Michaelsen (1922) from India possess enteroic nephridial system, unlike the type species Howascolex madagascariensis , which is exoic. Therefore he erected for these, and also several newly described species from India, a separate genus Wahoscolex Julka, 1988 leaving Howascolex from Madagascar monotypic.

In 2015 the second and third authors conducted earthworm collections in the Farafangana region, South Eastern Madagascar resulted in collecting two species attributable to the genus Howascolex. One species proved to be identical with H. madagascariensis Michaelsen, 1901, the other represents a species new to science and hitherto described.

Material and methods

Study area. The new collecting sites are situated at the Farafangana district, Vatovavy Fito Vinany region, South East Madagascar (Fig. 1).

Figure 1. 

Sampling localities in Madagascar. Black dot = H. madagascariensis type locality, black square = H. madagascariensis new record, black triangle = H. farafangana sp. n.

Methods. Earthworms primarily were collected by using the diluted formaldehyde method (Raw 1959) supplemented by digging and hand-sorting. The material collected was killed in 75% ethanol and fixed in 4% formaldehyde solution. From each morpho-species parallel material was conserved in 96% ethanol for DNA studies.

Deposition. The material collected is deposited in the Hungarian Natural History Museum(HNHM) and in the National Institute of Biological Resources(NIBR).


Family Acanthodrilidae Claus, 1880
Genus Howascolex Michaelsen, 1901

Howascolex madagascariensis Michaelsen, 1901

Howascolex madagascariensis Michaelsen, 1901: 202, Pickford 1937: 605, Julka 1988: 344.


Length 90–100 mm diameter 4–6 mm. Colour pale, pigmentation lacking. First dorsal pore in 12/13. Clitellum 13–19. ♀ 14 paired, presetal in a–a. Prostatic pores 17, 19. Spermathecal pores on the rim of 8 and 9, spermathecae with elongated oval ampoule, and a small duct bearing an acinous diverticula almost encircling the duct. Gizzard large in 5 or 6, last pair of hearts in 13. Calciferous glands large intramural encircles the oesophagus in 16. Excretory system holoic? before clitellum and meroic with 5–6 meronephridia and a stomate ventralmedian megameronephridium per side. Penial setae present. Ectal third highly bent, tip somewhat spoon-shaped. Length 2 mm diameter 0.04 mm, ornamentation small scattered teeth.

Material examined

ZMUH V5616 Howascolex madagascariensis syntypes 8 ex. S. Madagaskar, Andrahomana in Höhlen. Leg. Sikora.

HNHM/AF5667 1+1 juvenile ex., HNHM/AF5668 1 ex. Madagascar, Vatovavy Fito Vinany Region, Farafangana District, Tsararafa, Ankazomafaitsa 22°38'42"S, 47°50'04"E, 63 asl, Legit: Y. Hong & M. Razafindrakoto.


We had the possibility to examine the syntypes of Howascolex madagascariensis housed in the Zoological Museum of the University of Hamburg (ZMUH). The specimens are softened but all the inner structures are clearly seen. The nephridial system is completely identical with that of described in Michaelsen (1901). In the praeclitellar segments there is a pair of highly coiled stomate, exoic and avesiculate tubular holonephridium. In the postclitellar region the larger nephridia (megameronephridia) are accompanied by several smaller highly coiled meronephridia.

Our specimens agree well with the syntypes but their nephridia are not so well preserved and it seems that the praeclitellar holonephridium consists of 2–3 interconnected more compact regions which became separated after the clitellum to form 4–6 normal meronephridia. The shape of the spermathecae, the penial setae, and the distribution of the characteristic genital papillae are identical in the syntypes and the new material.

Howascolex farafangana sp. n.

Figs 2–6


Noon in apposition, refers to the type locality; Farafangana district, SE Madagascar.


External: Length of the Holotype 155 mm, width (postclitellar) 7 mm. Segments No. 205. Paratypes 142–150 mm in length and 6–7 mm in diameter, segment No. 186–228. Color greyish, pigmentation absent. Prostomium schizolobous, dorsal pores from 9/10. Segments from 3–12 bi- or triannulate, after clitellum with three or four ringlets. Setae visible from segment 2, eight per segment in closely paired regular rows. Setal formula after clitellum aa:ab:bc:cd:dd = 9.2:1.4:10:1:40 (Fig. 2). Setae a and b of 8, 9 modified to genital setae, of 17, 19 modified to penial setae. Spermathecal pores paired, presetal small slits on segment 8, 9 between ab. Clitellum saddle-shaped on 13–19. Female pores in 14, presetal and slightly lateral to b. Two pairs of prostatic pores in 17 and 19 just at the base of seta b, joined by slightly convex seminal grooves, running outside b. Male pores minute in 18, within the seminal grooves. Genital marks unpaired as 2–3 mid-ventral, intra and intersegmental papillar lines located in the region 19–22 and paired group of small postsetal papillae on 8, 9, 10, 12 in setal lines a–b (Fig. 3)

Figure 2–6. 

Howascolex farafangana sp. n. 2 Setal arrangements; a, b, c, d represent setal lines 3 ventral view of the fore-body; Fp = female pore, Gs = genital setal pore, Pap = genital papillae, Pp = prostatic pores, St = spermathecal pores (scale bar = 5 mm) 4 Penial seta, A = the whole seta, B = tip if the penial seta 5 Spermatheca (scale bar = 0.5 mm) 6 Genital seta, A = the whole seta, B = tip of the genital seta.

Internal: First septum visible 6/7, septa 8/9, 12/13–13/14 thickened, 9/10–11/12 strongly muscular. One large oesophageal gizzard in 5 or 6, extending up to segment 7. Dorsal vessel single throughout, last pair of hearts in 13. Excretory system with 2–3 coiled (interconnected?) exoic and stomate nephridial tufts per side before clitellum. After clitellum their number increases to 5–6 discrete biramous meronephridia and a ventral megameronephridium per side. Large intramural calciferous gland present in segment 16 sometimes bulging into segment 17 as well. Intestine begins in 20 bearing medium-sized lamellar typhlosole from 23. Lateral typhlosoles lacking.

Holandric. Two pairs of testes in 10, 11. Male funnels iridescent and plicated, testis sacs missing. Two pairs of seminal vesicles in 11 and 12, attached respectively to septa 10/11 and 11/12. One pair of moderate size ovaries in 13. Two pairs of tubular prostates of similar size in 17 and 19, highly coiled and confined to their own segment. Penial setae 3.5 mm in length and 0.025 mm in diameter. The ectal third bent, tip slightly lanceolate, ornamentation fine transversal serrations (Fig. 4).

Two pairs of spermathecae opening segmentally on 8 and 9. Ampulla slightly elongate, oval, duct short. Diverticulum front-facing, acinous, joins to the duct just above the spermathecal pore (Fig. 5). Genital setae almost straight, 1.8 mm long, and 0.035 mm in diameter. Tip lanceolate, ornamentation dense sharp scales (Fig. 6).


HNHM/AF5664. Madagascar, Vatovavy Fito Vinany, Farafangana, Tsararafa, Anrazomafaitsa. 22°43'35"S, 47°47'38"E, 28 m asl. Legit: Y. Hong & M. Razafindrakoto 20. 02. 2015.


HNHM/AF5665, 3 ex. Locality and date same as that of the Holotype. HNHM AF/5666, 2 ex. Madagascar, Vatovavy Fito Vinany, Farafangana, Tsararafa, Anrazomafaitsa 22°38'42"S, 047°50'4"E, 63 m asl. Legit: Y. Hong & M. Razafind-rakoto 18. 02. 2015.


This second species of Howascolex differs from the generotype by its larger size, the segmental spermathecal pores and in the presence of genital setae. The presence of a moderately sized typhlosole is also a difference, however the original description is erroneous reporting complete lack of typhlosole in H. madagascariensis. Opening the intestine just after the prostatic segments a small twine-like typhlosole can be observed running along the dorsal surface of the intestine.


The genus Howascolex was originally classified in the subfamily Octochaetinae within the highly heterogeneous family Megascolecidae, consisted also of Acanthodrilinae, Ocnerodrilinae and even Eudrilinae as subfamilies (Michaelsen 1900). The treatment of the subfamily Octochaetinae was quite heterogeneous in the subsequent revisions of the earthworms’ family system (e.g. Stephenson 1930, Lee 1959, Gates 1959, Jamieson 1971) until Sims (1980), mainly following Gates (1959), advocated a “pragmatic” solution elevating the previous subfamilies of the catch-all family Megascolecidae to family rank. In this system Octochaetidae was defined by the presence of tubular prostates in acanthodriline arrangement (basically two pairs of prostates in 17, 19, male pore in 18) and a meroic excretory system, while Acanthodrilidae differed from it only by its holoic nephridia.

This classical system was severely criticized by Csuzdi (1996, 2010) demonstrating that the meroic excretory system is highly homoplasious and therefore the family Octochaetidae so defined is polyphyletic. Although this view was not generally supported (e.g. Blakemore 2005, 2013) the accumulating molecular data suggest that the classical Octochaetidae is highly polyphyletic and the meroic states of the nephridial system were acquired independently in the different lineages (Buckley et al. 2011, James and Davidson 2012).

From this point of view the position of Howascolex is very interesting. Michaelsen (1901) and Stephenson (1930) hypothesized that Howascolex is basal to any other octochaetids with its composite (praeclitellar holoic and postclitellar meroic) excretory system. However it was noticed even by Michaelsen (1901) that the octochaetid Howascolex shows many similarities with the acanthodrilid species recorded by that time from Madagascar (Acanthodrilus majungianus Michaelsen, 1897 and Acanthodrilus voeltzkowi Michaelsen, 1897) e.g. the structure of spermathecae, the position of the last pair of hearts and the presence of post ovarial calciferous glands are all shared characters between these three species. Therefore he re-examined the nephridial system of the two acanthodriline species and recognized, that in voeltzkowi it is purely holoic, but in majungianus it cannot be determined due to the bad conservation.

The nephridial system of both species reported here is quite peculiar, consisting of very small repeatedly coiled tubes in the front of the body and a truly meroic system in the postclitellar segments. However, the similarity in the structure of spermathecae and also the presence of intramural calciferous glands in one or several post-ovarial segments suggest that they are closely related to the Malagasy acanthodriline species and the meroic excretory system evolved independently in the island. Consequently, the Howascolex and ‘Acanthodrilus’ species of Madagascar seem to form a monophyletic clade advocating also a rejection of the classical Octochaetidae family. To decide whether this scenario is right or Howascolex belongs to the Indian clade of octochaetid-like worms a detailed molecular study is needed.


We are grateful to Julia Philbert for her generous help during the fieldwork; Emma Sherlock (NHM, London) is thanked for polishing the English. This work was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2015R1D1A2A01057305).


  • Blakemore RJ (2005) Whither Octochaetidae? – its family status reviewed. In: Pop AA, Pop VV (Eds) Advances in Earthworm Taxonomy II. Cluj University Press, Cluj, 63–84.
  • Blakemore RJ (2013) The major megadrile families of the World reviewed again on their taxonomic types (Annelida: Oligochaeta: Megadrilacea). Opuscula Zoologica (Budapest) 44(2): 107–127.
  • Buckley TR, James S, Allwood J, Bartlam S, Howitt R, Prada D (2011) Phylogenetic analysis of New Zealand earthworms (Oligochaeta: Megascolecidae) reveals ancient clades and cryptic taxonomic diversity. Molecular Phylogenetycs and Evolution 58(1): 85–96. doi: 10.1016/j.ympev.2010.09.024
  • Černosvitov L (1939) Oligochaeta VIII. Résultats scientifiques des croisières du Navire-École Belge «Mercator». Mémoires du Musée Royal d’Histoire Naturelle de Belgique 15: 115–129.
  • Csuzdi Cs (1996) Revision der Unterfamilie Benhamiinae Michaelsen, 1897 (Oligochaeta: Acanthodrilidae). Mitteilungen aus dem Zoologischen Museum Berlin 72: 347–367. doi: 10.1002/mmnz.19960720219
  • Csuzdi Cs (2010) A monograph of the Paleotropical Benhamiinae earthworms (Annelida: Oligochaeta, Acanthodrilidae). Pedozoologica Hungarica No. 6. Hungarian Natural History Museum, Budapest, 348 pp.
  • Gates GE (1959) On a taxonomic puzzle and the classification of the earthworms. Bulletin of the Museum of Comparative Zoology at Harvard College 12(6): 229–261.
  • Gates GE (1962) On some earthworms of Eisen’s collection. Proceedings of the California Academy of Sciences 31(8): 185–225.
  • Graff O (1957) Regenwürmer aus El Salvador (Oligochaeta). Senckenbergiana Biologica 38: 115–143.
  • James SW, Davidson SK (2012) Molecular phylogeny of earthworms (Annelida : Crassiclitellata) based on 28S, 18S and 16S gene sequences. Invertebrate Systematics 26: 213–229. doi: 10.1071/is11012
  • Jamieson BGM (1971) A review of the Megascolecoid earthworm genera (Oligochaeta) of Australia. Part I. Reclassification and checklist of the Megascolecoid genera of the world. Proceedings of the Royal Society of Queensland 82(6): 75–86.
  • Julka JM (1988) Fauna of India. Megadrile Oligochaeta (Earthworms). Family Octochaetidae. Zoological Survey of India, Calcutta, 400 pp.
  • Lee KE (1959) The earthworm fauna of New Zealand. New Zealand Department of Scientific & Industrial Research Bulletin 130, 486 pp.
  • Michaelsen W (1900) Oligochaeta.Das Tierreich X, Frieländer und Sohn, Berlin, 575 pp.
  • Michaelsen W (1901) Oligochäten der Zoologischen Museum zu St. Petersburg und Kiew. Bulletin de l’Académie Impériale des Sciences de St. Pétersbourg 15: 136–215.
  • Michaelsen W (1922) Oligochäten vom westlichen Vorderindien und ihre Beziehungen zur Oligochätenfauna von Madagaskar und den Seychellen. Mitteilungen aus dem Naturhistorischen Museum in Hamburg 38: 27–68.
  • Pickford GE (1937) A Monograph of the Acanthodriline Earthworms of South Africa. Heffer & Sons, Cambridge, 612 pp.
  • Sims RW (1980) A classification and the distribution of earthworms, suborder Lumbricina (Haplotaxida: Oligochaeta). Bulletin of the British Museum (Natural History) Zoology 39: 103–124.
  • Stephenson J (1930) The Oligochaeta. Clarendon Press, Oxford, 987 pp.
login to comment