Pelodrilidae, Martin & Fend & Martinsson & Klinth & Torii & Erséus, 2024

Martin, Patrick, Fend, Steven, Martinsson, Svante, Klinth, Mårten, Torii, Takaaki & Erséus, Christer, 2024, Towards an integrative revision of Haplotaxidae (Annelida: Clitellata), Zoological Journal of the Linnean Society (zlae 141) 202 (4), pp. 1-38 : 13-14

Pelodrilidae fam. nov. (clade 2 in Fig. 1 )

ZooBank LSID: urn:lsid:zoobank.org:act:67210344-489D-458F-9CC7-D9EE83952089

Type genus: By original designation, Pelodrilus Beddard, 1891 .

Diagnosis

Body form not unusually narrow and elongate, cuticular layer thin, peristomium not elongate, brain in peristomium. Chaetae 4 pairs per segment, usually simple-pointed, but may have distal ornamentation or keel; dorsal chaetae not much smaller than ventrals, present in most or all segments. Pharynx with an eversible dorsal pad; conspicuous pharyngeal glands present. Nephridia present in some, but not all segments; ducts elongate-tubular, of various forms, but not forming a dense mass filling much of the segment. Dorsal and ventral blood vessels connected by simple commissural vessels. Clitellum one cell thick. Spermathecae anterior to gonadal segments. Two pairs of testes; one or two pairs of ovaries with the second pair being lost where reduction has occurred; eggs mesolecithal. Gonoducts simple, without attached prostate glands, but there may be glands around the pores; male ducts tubular, usually plesioporous.

Remarks

This proposed family is most closely associated with megadriles (Metagynophora, Opisthopora , Crassiclitellata Jamieson, 1988 ) by the molecular evidence. Although members of Pelodrilidae may be large and thick-bodied, they differ morphologically in several respects from typical megadriles: (i) the clitellum is relatively thin, composed of a single cell layer, (ii) the brain is in the peristomium, (iii) the lateral blood vessels are simple commissures, (iv) eggs are large and yolky (mesolethical), (v) male ducts are usually plesioporous (not opisthoporous sensu Michaelsen ), and not embedded in the body wall, and (v) ovaries are in GIII (progynous, rather than metagynous).

Genera: Pelodrilus Beddard, 1891 (type species, Pelodrilus violaceus Beddard, 1891 ); Hologynus Brinkhurst, 1988 (type species, Pelodrilus hologynus Michaelsen, 1907 ); Delaya Brinkhurst, 1988 (type species, Pelodrilus bureschi Michaelsen, 1925 ). [Incertae sedis: Alphadrilus Brinkhurst, 1988 (type species, Phreoryctes smithii Beddard, 1888 ); Adenodrilus Čekanovskaja, 1959 (type species, Adenodrilus denticulatus Čekanovskaja, 1959 ); Heterochaetella Yamaguchi, 1953 (type species, Heterochaetella glandularis Yamaguchi, 1953); and Omodeodrilus Kammerer, 2006 (type species, Villiersia guanivora Omodeo, 1987 )].

Morphologically examined material: Hologynus cf. hologynus (Michaelsen, 1907) : WAM V12029 and V12030 : Western Australia, Manjimup, south of Pemberton, Spring Gully at Gloucester Rd. ; two slide-mounted anterior ends ( CE17254– 17255 ). Pelodrilus cf. darlingensis Michaelsen, 1907 , WAM V9004 : South Western Australia, Augusta-Margaret River Region , Upper Margaret River , south of Busselton , Rapids Conservation Park , Canebrake Pool : one slide-mounted, anterior end ( CE17262 ). All this material collected 16 Sep 2012 by C. Erséus, A. Pinder, and Y.-D. Cui. For more details, see also Table 1 and Supporting information, Table S1 .

Delaya species in the molecular analyses were not examined for morphology. They have a very similar general appearance and internal anatomy, making them difficult to identify. Their identification is essentially based on subtle chaetal characteristics (ornamentation and position) and the presence of species complexes cannot be excluded, especially for a species such as Delaya bureschi ( Michaelsen, 1925) , which has a wide geographical distribution ( Greece, Slovenia, Bulgaria, Romania, Macedonia; Hrabě 1963, Botea and Botoşaneanu 1966, Delay 1970, Juget and Dumnicka 1986, Giani et al. 2001). Hence, the identification of the specimens of Delaya leruthi ( Hrabě, 1958) (CE13922) and D. bureschi (CE33796) is made on a provisional basis and relies more on their presence in caves where their population has been known and followed for many years ( D. leruthi : L’Estelas cave, France, Delay 1970, D. bureschi : Mrzla cave, Slovenia, Hrabě 1963) than on morphological examination. The unidentified species Delaya spIT (CE7161) and Delaya spGR (CE33797) were attributed to this genus by their genetic similarity to the other two taxa.

Descriptive notes

The specimens identified as Hologynus cf. hologynus in the present analysis have a dorsal pharyngeal pad in II-1/2III, and large pharyngeal glands in V–VI (smaller in VII–VIII) (Supporting information, Fig. S3A ). As noted by Brinkhurst (1966), there is no secondary annulation. The single pair of spermathecae has pores on the lateral lines at 6/7; the ampullae are quite elongate, extending back into VIII, as described for both Hologynus hologynus [ Brinkhurst 1966 and Benham 1909 (as Pelodrilus aucklandicus )] and Hologynus bipapillatus ( Michaelsen, 1925) . The worms are hologynous, with ovaries in XII and XIII, and female pores intersegmental on 12/13 and 13/14 (Supporting information, Fig. S3B ). The anterior male ducts are clearly plesioporous, with pores just posterior to ventral chaetae of XI (Supporting information, Fig. S3C ); the posterior male ducts are just behind intersegment 11/12 (indistinctly plesioporous); both pores are adjacent to secretory surfaces of ventral gland clusters.

The probable Pelodrilus specimen analysed here is partially mature, with one pair of rudimentary spermathecal pores on the lateral line, at 7/8. The dorsal pharyngeal pad and extensive pharyngeal glands ( Fig. 2F ) are similar to those of Hologynus hologynus . There are partially developed gonads in X–XII (most likely testes in X and XI and ovaries in XII), and rudimentary female funnels appear to be developing on 12/13. The location of the spermathecal pores at 7/8, as well as the apparent ovaries in XII only (progynous condition) is consistent with Pelodrilus darlingensis Michaelsen, 1907 , and these characters distinguish it from Hologynus species.

Remarks

Our Pelodrilus specimen was collected about 100 km south-west of the type locality of P. darlingensis , in a town called Collie, and the Hologynus collection site was about 200 km south of the type locality for Hologynus hologynus , near Yarloop, Western Australia.

We are unable to find a clear apomorphy for the widespread (but well-supported) Clade 2, represented by both Palaearctic ( Delaya ) and Australasian ( Pelodrilus and Hologynus ) species in the present analysis. These worms all have a dorsal pharyngeal pad in II-1/2III, and large pharyngeal glands from about V to VIII, and there is no ‘gizzard’ ( Fig. 2F ; see also Michaelsen 1907, Benham 1909, Hrabě 1958). Anterior gut morphology thus differs markedly from Haplotaxidae s.s. as defined here ( Fig. 2A–C ) but appears to be typical for microdrile oligochaetes.

Although the male ducts are quite simple, and usually plesioporous, members of the family show some variation in reproductive characters. For example, the posterior pair of male pores in Hologynus is shifted anteriad within the segment (Michaelsen 1907, 1924, Benham 1909), and may even enter the preceding segment (i.e. the prosoporous condition, resembling what is seen in Lumbriculidae , Branchiobdellida , and Kurenkovia Sokolskaja, 1969 ). In contrast, Pelodrilus violaceus Beddard, 1891 may show a rearward shift of the anterior male pores to a position ahead of the posterior pores on XII, approaching an opisthoporous condition, typical for megadrile families ( Beddard 1891: figs 22, 27). The second ovarian segment is absent (the progynous condition, as in typical microdriles) in Pelodrilus species, unlike other (hologynous) members of the group ( Brinkhurst 1988). Species of both Pelodrilus and Hologynus tend to have a reduced number of spermathecal segments (one or two) compared with other ‘ Haplotaxidae s.l. ’, whereas Delaya may have three or four ( Brinkhurst 1966). Brinkhurst (1988) was unable to find a clear autapomorphy for Delaya , although all species have keeled or ornamented chaetae and plesioporous female ducts; the various species are separated by number of spermathecae and cutaneous/sexual glands, position of chaetal bundles, and details of chaetal morphology ( Delay 1972, 1973).

It should be noted that the molecular analysis does not support inclusion of the morphologically similar Ohtakiana kakidaensis (described below) from Japan (= Clade 4) in this clade, but rather associates it with the Lumbriculidae and Hirudinea-like taxa. The simple male ducts and general (unremarkable) body form of Ohtakiana resemble those of Pelodrilidae as defined above, but also resemble those of several additional taxa listed above as ‘ incertae sedis ’—all of which are rare and monotypic, and unavailable in this study. These taxa also generally resemble Pelodrilidae in other typical microdrile characters, e.g. paired chaetae, eversible pharynx with pharyngeal glands.

As a whole, i.e. including all the genera we have listed as putative members, the family Pelodrilidae has a wide distribution in the world. Taxa included in the present analysis were Australasian representatives of Pelodrilus and Hologynus , plus the Palaearctic Delaya . Additional Pelodrilus species have been described from the Afrotropical ( Pelodrilus africanus Michaelsen, 1905 ) and Palaearctic ( Pelodrilus ignatovi ) regions; however, it should be noted that the latter was regarded as atypical by Brinkhurst (1988). Of the remaining genera not analysed here Omodeodrilus is Afrotropical, Heterochaetella and Adenodrilus are Palaearctic, and Alphadrilus is Australasian.

Figures

Figure 1. Phylogenetic tree of Clitellata estimated with Bayesian inference in MrBayes, using a concatenated set of markers, i.e. 12S, 16S, COI, 18S, and 28S. The tree is rooted such that Parvidrilidae and Randiellidae (also Clitellata) appear as lineages outside the rest of the ‘Clitellata’ tree, a position strongly supported by the metagenomic analyses of Erséus et al. (2020). Haplotaxid like taxa are shaded.Support values at branches are posterior probabilities, scale represents expected number of changes/site. Capital letters at the end of the species codes in Haplotaxis indicate countries of origin.BEN: Benin, FR: France, GR: Greece, IT: Italy, JP: Japan, SE: Sweden, US: USA. Inset, photo of live specimen of Haplotaxis spSE in its natural habitat, soil soaked in groundwater, photo: Johan Wingborg, and photo of live specimen of Haplotaxis spBEN6, photo: Patrick Martin.

Figure 2. Comparison of anterior ends of haplotaxid-like worms analysed here, schematic figures with emphasis on somatic characters. C, F, and H are from the genetically analysed specimens, the other figures are based on individuals from the same site (and usually same date) as the analysed worms, but better fixed for morphology. A, Haplotaxis spUS2 from Corral Creek, Idaho, USA.Oral cavity of gut is contracted, muscular pharynx extends through two segments.B, Haplotaxis spJP2 from Gudari-numa, Aomori, Japan.Oral cavity of gut is expanded, muscular pharynx is shorter than in the Idaho specimen. C, Haplotaxis spJP1 from Kakida River, Shizuoka, Japan.Timm’s glands are larger than in (A) or (C), muscular pharynx is short.D, Haplotaxoides decipiens from Guadalupe Creek, California, USA.E, Ohtakiana kakidaensis from Kakida River, Shizuoka, Japan. F, Pelodrilus cf. darlingensis from Western Australia. G, Limpluvia setoensis from Asahina River, Shizuoka, Japan. H, undetermined Lumbriculidae, specimen CE32192, from Euchre Creek, Oregon, USA.

Figure3.Haplotaxis species,somaticcharacters.A,Haplotaxis spUS2 fromCorral Creek,Idaho,USA.B,D–H,unidentifiedHaplotaxis sp.(population notanalysed genetically) fromsprings near Brewer,Montana,USA.C, I, Haplotaxis spUS3from Guadalupe Creek,California,USA.J,unidentified Haplotaxis sp.(population not analysedgenetically) from StonyCreek,California,USA.A, anteriorend ofdissected worm,showing extensive musculaturebetween gut and bodywall in I–III,and thick-walledmuscular pharynx in IV–V.B,sagittal section,showingthin-walled oral cavity (right, anterior) and contracted,muscular pharynx (left,posterior).C, wholemounted worm, showingpartially contracted oral cavity and muscular pharynx, and secondary annulationbeginning in V.D,sagittal section ofa contracted muscular pharynx,with central band ofcircularmuscles,surrounded by region with more radial muscles.E, F,sagittal sections ofmiddle and posterior regions showing gut wallwith extensive chloragogen layer.G, sagittal section oftwo middle segments showingextensive nephridia.H, sagittal section,showing Timm’sgland beneath ventral nerve cord.I, smalldorsal and large ventral chaeta (with a partially developedventral chaeta) in mid-bodysegment.J,ventral chaeta frommid-body segment.