Leaniricola rotundata M'Intosh 1885

Leaniricola rotundata M’Intosh, 1885

(Figs. 2–6)

Original description. M’Intosh (1885): 153–154; Fig. 2.

Host. Sthenolepis areolata (M’Intosh, 1885) [as Leanira areolata M’Intosh, 1885] (family Sigalionidae).

Type locality. Embedded in the base of a parapodium of the predatory scale worm, S. areolata, trawled at H.M.S Challenger station 232; south of Tokyo (formerly known as Yedo), Japan, 35º11’ N, 139º28’ E; depth 345 fathoms (631 m); green mud.

Material examined. The holotype ♀ preserved in ethanol (NHMUK reg. no. 12.5.1875) proved heavily damaged and worthless for descriptive purposes. Inspection of the holotype of Leanira areolata (NHMUK reg. no. 85.12.1.116) revealed a second female specimen of L. rotundata which was found embedded between its parapodia and is used for the redescription below; collected 12 May 1875.

Redescription of female. Body almost spherical in dorsal aspect (Fig. 2 A), maximum width 2,340 µm; consisting of bulbous prosome and slender, ventrally reflexed urosome (Fig. 3 A); total body length 4,670 µm, measured along dorsal curvature from anterior margin of prosome to posterior margin of caudal rami.

Cephalosome separated from remainder of prosome by bilateral constriction (Fig. 2 A), no functional articulation; triangular in dorsal aspect, with rounded posterolateral angles bearing spinulose pads (Fig. 2 A, B); dorsal and lateral surfaces with sensillar pattern as illustrated in Figs. 2 A and 3A. Rostrum (Fig. 2 A) offset, forming trapezoid projection, fused at base.

Somites bearing legs 1–4 fused, forming bulbous mid-region; no sensillae discernible; region equivalent to somite bearing leg 4 reflexed ventrally, separated from urosome by fully functional articulation (Fig. 3 A, C).

Urosome (Fig. 3 A–C) not visible in dorsal aspect, 6-segmented, comprising two wide thoracic and four narrow abdominal somites. First thoracic somite limbless (leg 5 not expressed), expanded dorsally forming lobate protrusion. Second thoracic (= genital) somite with paired dorsolateral genital apertures; genital opercula unarmed. Abdominal somites 3–4 fused ventrally, fully separated dorsally (Fig. 3 B, C); anal somite with small unarmed operculum (Fig. 3 B). Paired egg sacs large, sausage-shaped (Fig. 2 A).

Caudal ramus (Figs. 3 B, C; 4C, D) elongate, about 3.2 times as long as wide; distal portion forming ventrally recurved lobate outgrowth covered by four spinulose pads; dorsolateral pore present near outer margin. Each ramus with five naked setae (setae I and VII apparently absent); seta V longest and not fused at base to setae IV or VI.

Antennule (Fig. 5 A) slender, 6-segmented; segment 2 longest. Armature formula: 1-[3 + 1 multipinnate], 2-[7 + 4 multipinnate], 3-[5 + 1 multipinnate], 4-[5], 5-[2 + aesthetasc], 6-[6 + aesthetasc]. Multipinnate elements spiniform, distalmost one on segment 2 particularly strong.

Antenna (Fig. 5 B) 4-segmented, comprising large coxobasis and 3-segmented endopod. Coxobasis without ornamentation. Enp-1 with one small, minutely pinnate seta; without surface ornamentation. Enp-2 with large spinulose pad, two naked setae and one large, finely pinnate, recurved spine. Enp-3 small, partly embedded in enp- 2; with three geniculate setae (with fine spinules distal to flexure point), one large multipinnate seta, one short naked seta and one finely pinnate, recurved seta.

Labrum with large, anteriorly directed cylindrical extension with bilobate apex, forming anterior face of oral cone (Fig. 4 A, B); discernible in dorsal aspect (Figs. 2 A; 3A); with paired lateral folds embracing proximal halves of mandibular gnathobases (Fig. 4 A).

Mandible (Fig. 4 A, B) very large and of extraordinary shape; palp absent. Gnathobases entering oral cone via slit between labrum and labium and forming strongly chitinized, cylindrical extensions, produced distally into massive, three-dimensionally expanded anchors with serrated medial margin.

Paragnaths fused forming medially pointed lobe (labium) at base of posterior face of oral cone (Fig. 4 A).

Maxillule (Fig. 4 A, B) small, 1-segmented; with three apical setae.

Maxilla (Fig. 5 C) 2-segmented, comprising syncoxa and allobasis. Syncoxa large, expanded basally and with large spinulose pad along distal half of outer margin; unarmed. Basis an elongate segment, partly embedded in syncoxa; with one strong, straight apical claw and one small accessory element near its base; claw slightly bifid near apex.

Maxilliped (Fig. 5 D) 3-segmented, comprising syncoxa, basis and endopod. Syncoxa robust, without ornamentation. Basis elongate, unarmed, with spinulose pad halfway along outer margin. Endopod represented by strong elongate claw (longer than basis) with minute serrations along distal quarter of inner margin; with one vestigial accessory element plus pore near base of claw.

Leg 1 (Fig. 6 A) biramous, endopod medially directed. Praecoxa and coxa well developed, without surface ornamentation. Basis with two spinulose pads on anterior surface and few spinules near insertion site of outer naked seta. Exopod 2-segmented, segments subequal in length; exp-1 with spinules around outer margin and at base of outer recurved spine; exp-2 with numerous spinules around outer margin and few setules around proximal inner margin, armature consisting of four bipinnate spines (proximal one with recurved tip, others with flagellate extension) and three bipinnate setae. Endopod 2-segmented; enp-1 shortest and widest, with inner bipinnate seta and spinulose pad around outer margin; enp-2 with one recurved bipinnate spine and four bipinnate setae, and spinules around outer margin and bases of outer spine and apical setae.

Leg 2 (Fig. 6 B) biramous, endopod medially directed. Praecoxa not discernible. Coxa large, without ornamentation. Basis with spinulose pad on anterior surface near insertion of exopod; outer basal seta naked. Exopod 2-segmented; exp-1 shortest, with spinules around outer margin and at base of outer recurved spine; exp-2 with numerous spinules around outer margin and few spinules around proximal inner margin, armature consisting of two recurved spines and four bipinnate setae. Endopod 2-segmented; enp-1 shortest, with bipinnate inner seta and spinulose pad around outer margin; enp-2 with three recurved bipinnate outer spines and two bipinnate inner setae, and spinules around outer margin and bases of spines.

Leg 3 (Fig. 6 C) uniramous, 2-segmented, comprising undivided protopod and exopod; leg members widely separated and discernible in dorsal aspect (Fig. 2 A). Protopod fused at base to somatic wall; with naked outer basal seta surrounded at base by few spinules. Exopod a single ovoid segment covered anteriorly by spinulose pad in distal half and with long multipinnate seta.

Leg 4 (Fig. 6 D) vestigial, represented by ovoid segment with spinulose pad on anterior surface; anteriorly directed (Fig. 2 A, C).

Leg 5 absent.

Male. Unknown.

Remarks. Leaniricola differs from all known extant cyclopoid genera by the presence of an oral cone, making it a chimaera displaying both siphonostome and poecilostome characters. However, L. rotundata cannot be placed in the Siphonostomatoida based on the segmentation pattern of the female antennule and the morphology of the antenna. The distal part of the female antennule in siphonostomatoids is characterized by the presence of an aesthetasc on ancestral segment XXI and the absence of the boundary between ancestral segments XXIV and XXV (these segments forming a double or even more compound segment) (Huys & Boxshall 1991; Boxshall & Huys 1998). In L. rotundata aesthetascs are present on segments XXV and XXVIII but not on segment XXI (Fig. 5 A) and segment XXV is expressed as a free segment while segment XXIV is incorporated into a more proximal quadruple segment (XXI–XXIV). The penultimate antennulary segment (XXV) of all copepodid stages of almost every poecilostomatoid thus far recorded is expressed as a distinct segment and carries a seta and an aesthetasc anterodistally and a seta posterodistally (Boxshall & Huys 1998). This free segment represents a characteristic signature for the poecilostome families in the Cyclopoida. The antennary armature in siphonostomatoids is sparse. In species that have retained the 3-segmented condition of the endopod the first segment is always unarmed, the second carries a single seta and the third has a maximum of four setae, one commonly claw-like, around the distal margin. In L. rotundata the first segment carries a seta, the second has three elements and the third six elements around the apex. This armature pattern, in conjunction with the fusion of the coxa and basis into a coxobasis and the absence of the exopod, is reminiscent of the poecilostome condition.

The oral cone of siphonostomatoids is formed from the anterior lip, the labrum, and the posterior lip, the labium which represents the paired paragnaths. A genuine oral cone has evolved independently in some harpacticoid families such as the Superornatiremidae and Novocriniidae (Huys 1996; Huys & Iliffe 1998) but has thus far not been reported in the Cyclopoida. Buccal cone-like structures have been observed in the unplaced genus Endocheres Bocquet & Stock, 1956 (Boxshall & Halsey 2004) and in members of the Lamippidae (Stock 1988) but their homology with the oral cone of siphonostomatoids and Leaniricola is questionable. The labrum and labium are only loosely associated in L. rotundata and part readily to allow movement of the mandibular gnathobases between them. The larger part of the oral cone is formed by the muscular labrum with the labium only contributing to its basal section. The female specimen examined in this study was found embedded between the parapodia with its oral cone penetrating the integument of its polychaete host. Presumably the massive, three-dimensionally expanded mandibular gnathobases serve a dual function as feeding appendages as well as anchoring devices. However, it is not known how the oral cone is used to penetrate the host and how nutrients are transported back to the oesophagus.

Although the taxonomic history of the genus Leaniricola has been contentious since its inception, most authors have traditionally associated it with the Nereicolidae (M’Intosh 1885; Gooding 1963; Stock 1968; Boxshall & Halsey 2004; Conradi et al. 2015). The family currently includes 19 species in seven genera (Boxshall & Halsey 2004; Kim et al. 2013) all of which exclusively utilize polychaetes as hosts: Nereicola, Selius Krøyer, 1837; Selioides Levinsen, 1878; Anomopsyllus Sars, 1921; Pherma Wilson, 1923; Sigecheres Bresciani, 1964 and Vectoriella Stock, 1968. The distinction between Selius and Selioides is based solely on the assumption that Krøyer‘s (1837) observation of the maxilliped is correct. The inadequately described Chelonidiformis Hesse, 1869 is not considered here since it is currently considered a genus inquirendum (Boxshall & Halsey 2004). Although there is a superficial similarity in gross body morphology, particularly when viewed in dorsal aspect, between Leaniricola and members of Nereicola, Selius and Selioides (cf. Krøyer 1837; Keferstein 1863; Laubier 1965; Carton & Laubier 1974; Stock 1996) the nereicolid genera are characterized by a strongly reduced urosome which is not reflexed under the prosome as in L. rotundata.

The antenna of L. rotundata is 4-segmented, comprising a coxobasis and a 3-segmented endopod. Most nereicolid genera (Anomopsyllus, Nereicola, Pherma, Selioides, Sigecheres) typically share the apomorphic condition in which the middle and distal endopodal segments are fused, forming a 3-segmented antenna. A further derived state is displayed by Vectoriella which has a strongly reduced 1-segmented antenna; the condition in Selius is unconfirmed. The maxillary basis in members of the Nereicolidae and Clausiidae typically has a rounded tip armed with a spinulose pad (and sometimes with up to two accessory ones). This diagnostic synapomorphy is absent in Leaniricola which has a straight apical claw, indicating that the genus cannot be accommodated in either of these annelidicolous families. Based on the presence of an oral cone and the unique morphology of the mandibular gnathobases it is here fixed as the type genus of a new family, Leaniricolidae fam. nov.

According to M’Intosh (1885) a form similar to L. rotundata was found on Leanira hystricis Ehlers, 1874 from the south-west of Ireland. In one of the ‘Porcupine’ 1869–1870 expedition reports dealing with the sigalionid polychaetes, M’Intosh (1876: 409) does indeed state “ At the anterior end of a fragmentary specimen is apparently a crustacean parasite immersed in the dorsal muscles”. However, inspection of this material (four specimens in a bad condition; M’Intosh collection; NHMUK reg. no. 1921.5.1.653) collected off the south-west coast of Ireland at 808 fathoms (1,478 m) depth revealed no additional copepods. The host genus Sthenolepis Willey, 1905 belongs to the family Sigalionidae in the infraorder Aphroditiformia (order Phyllodocida). Only two other aphroditiform families serve as hosts to copepods. The Polynoidae (Conradi et al. 2015) are most commonly infested by annelidicolous copepods, including members of the Herpyllobiidae (e.g. Lützen 1964; Stock 1986, 1996; López-González et al. 2000, 2006), Nereicolidae (e.g. Carton 1965; Bresciani 1967; Carton & Laubier 1974; Stock 1986, 1996) and occasionally (and probably accidentally) Sabelliphilidae (Bocquet et al. 1963). One species of the aphroditiform family Acoetidae serves as host to the catiniid Cotylemyzon vervoorti Stock, 1982. Leaniricola rotundata is so far the only copepod that utilizes a sigalionid host.