Flabellicola Gravier, 1918a

Huys, Rony, 2016, Enigmas from the past: M’Intosh’s (1885) annelidicolous copepods from the voyage of H. M. S. Challenger, Zootaxa 4174 (1), pp. 355-385 : 379-380

Flabellicola Gravier, 1918a

The monotypic genus Flabellicola was described by Gravier (1918a) from specimens, at different stages of development, parasitic on the flabelligerid polychaete Flabelligera diplochaitos ( Otto, 1821) in the Gulf of Naples. Although being abundant at the type locality, particularly during April-May when prevalence can be up to 50% ( Gravier 1918b), the parasite has not been recorded again since its original description. Adult females of Flabellicola neapolitana Gravier, 1918a are mesoparasitic and typically embed themselves in the gills, located dorsally between the two chaetal bundles that form the cephalic cage. Interestingly, similar to the flabelligerid host utilized by Bradophila , their presence is betrayed by the paired egg sacs which extend into the cephalic cage of the polychaete. The pyriform ectosoma is about 0.30–0.35 mm in size (measured along its longest axis) and connects via a short neck-like region (stalk) to an internal vesicle (endosoma) which is about twice the length of its external counterpart. Embedded females lack all trace of appendages, digestive tract and external segmentation; however, the endosoma appears to display a transverse constriction dividing it in an anterior and a posterior part ( Gravier 1918b). The ovaries are located in the anterior part where they connect to paired oviducts that transport the developing eggs via the remainder of the endosoma and connecting stalk to the external genital apertures of the ectosoma. The paired multiseriate egg sacs are very large, attaining 1.06 mm in size (or over three times the length of the ectosoma). It is not uncommon to observe up to five parasites on the gills of a single host but only the larger specimens are ovigerous. Other females at an earlier stage of development are completely embedded in the branchial tissues and appear to be more numerous than those that have a protruding ectosoma. Gravier (1918a, 1918b) failed to observe males but found spermatozoa, presumably stored in a seminal receptacle, in cross-sections of the female’s ectosoma. Contrary to some published claims ( Bresciani & Lützen 1966: 804; Gotto 1979: 34) Gravier did not infer that F. neapolitana was a self-fertilizing hermaphrodite as previously (but incorrectly) proposed for Xenocoeloma alleni ( Brumpt, 1897) ( Caullery & Mesnil 1919) but concluded that the sperm must have been introduced by an as yet undiscovered male. Based on a series of histological sections Gravier (1918a, 1918b) attempted to reconstruct the female pathway of the life cycle. Although the infective stage is as yet unknown he assumed that it penetrated the host and developed inside the gill tissues. Developing females lack a functional gut and probably absorb nutrients directly through their specialised integument while eggs start developing and gradually fill up the oviducts. At sexual maturity the female penetrates the host integument a second time and protrudes the ectosoma while remaining attached inside with the endosoma. After mating and fertilization, eggs are deposited formings large paired egg sacs and probably remain attached until eclosion takes place. The proposed life cycle is somewhat similar to that of female splanchnotrophids which also penetrate the body wall of their host twice; however, in F. neapolitana mating presumably takes place outside the polychaete host while in members of the Splanchnotrophidae it occurs inside the viscera of the nudibranch gastropod ( Huys 2001).

Gravier (1918a, 1918b) compared Flabellicola with other genera that were known to utilize flabelligeran polychaetes as hosts, claiming that it was probably closest to Trophoniphila. Although he suggested a certain affinity with the Herpyllobiidae the genus remained unplaced (cf. Gotto 1979) until Boxshall & Halsey (2004) treated it as a genus inquirendum in the Saccopsidae . The complete absence of appendages on the female ectosoma, the size and shape of the egg sacs and its utilization of a flabelligerid polychaete as host suggest a possible relationship with the Bradophilidae rather than with the Saccopsidae which typically have three pairs of reduced cephalic appendages, much smaller, sausage-shaped or straight egg sacs and utilize ampharetids, terebellids and trichobranchids as hosts ( Sars 1870; Levinsen 1878; M’Intosh 1885; Bresciani & Lützen 1961, 1975). Consequently, Flabellicola is here treated as a genus incertae sedis in the Bradophilidae .

The positioning of the ovaries in the endosoma of Flabellicola rather than in its ectosoma is unusual in mesoparasitic copepods and has so far only been observed in the recently discovered Jasmineiricolidae ( Boxshall et al. 2015) . Whether this character is also diagnostic for the Bradophilidae remains to be confirmed since Marchenkov (1999b, 2002) did not comment on the position of the ovaries in Bradophila and no information is available on the condition in Trophoniphila.

Flabelligerid polychaetes are rarely reported as hosts for parasitic copepods. The most important diagnostic feature of flabelligerids is their ability to retract the anterior end, including the pro- and peristomium with associated palps and gills, and some of the anterior chaetigerous segments into the body, forming an introvert ( Filippova et al. 2003). This confined microhabitat is the preferred attachment site for the three mesoparasitic members of the Bradophilidae . The only other copepod that is known to utilize a flabelligerid host is Flabelliphilus inersus Bresciani & Lützen, 1962 , which was described from off the Swedish west coast (Bresciani & Lützen 1962) but has no bradophilid affinities and occupies a different niche on the host. The species inhabits the gelatinous coat of Flabelligera affinis M. Sars, 1829 , is known from males only and generally considered of doubtful systematic position due to the incomplete description. Stock (1968) listed Flabelliphilus Bresciani & Lützen, 1962 as a genus inquirendum in his “nereicolid series” but Laubier (1978) regarded a position in the Nereicoliform Group unlikely. Bresciani (1964) had previously considered it a possible candidate for inclusion in the Clausidiidae . Boxshall & Halsey (2004) ranked it as a genus inquirendum based on the clausiid-like antenna and mandible while subsequent workers cited it as a valid genus of this family ( Cheng et al. 2014; Conradi et al. 2015).