Diogenion cf. vermifactus Codreanu, Codreanu & Pike, 1960

Detorre, Marissa, Williams, Jason D. & Boyko, Christopher B., 2023, A review of the endoparasitic isopods (Epicaridea: Entoniscidae) from hermit crabs, including description of the new subfamily Diogenioninae and a new species of Paguritherium Reinhard, 1945 from the Philippines, Zootaxa 5249 (1), pp. 12-40 : 17-20

Diogenion cf. vermifactus Codreanu, Codreanu & Pike, 1960

Figures 3–5

Diogenion vermifactus Codreanu, Codreanu & Pike, 1960: 439–441 , fig. 1 (Red Sea, infesting Diogenes senex ); Codreanu et al. 1965: 225 (mention); Codreanu 1967: 209 (mention); Bourdon 1980: 243 (list); Adkison 1990: 34–40, fig. 3 (after Codreanu et al. 1960); Kensley 2001: 226 (list); McDermott et al. 2010: 12 (list), 28 (mention).

unidentified entoniscid Williams et al. 2019: 85, 97, 101, 104 ( Philippines, infesting Calcinus gaimardii and Calcinus minutus ).

Material examined. Philippines: Female (19.4 mm) ( USNM 1522331), infesting Calcinus gaimardii (3.5 mm SL), inhabiting unknown shell, Lalaguna Beach, Puerto Galera, 13°31’32″ N, 120°58’8″ E, coll. J.D. Williams, 3 March 1999. Female (6.9 mm), male (2.5 mm), and multiple larvae on two SEM stubs ( USNM 1522332), infesting Calcinus pulcher (3.5 mm SL), inhabiting unknown shell, Batangas, Anilao, 13°42’14.5″ N, 120°52’45.3″ E, coll. J.D. Williams, 13 February 1999. Female (19.0 mm) ( USNM 1522333), infesting C. gaimardii (6.0 mm SL), inhabiting unknown shell, Mabayo, Bataan, 14°44′00″ N, 120°16′32″ E, coll. J.D. Williams, 21 February 1999. Female (10.5 mm) and male (2.5 mm) ( USNM 1522334), infesting Calcinus minutus (2.7 mm SL), inhabiting unknown shell, host also with bopyrid parasite ( Bopyrissa marami ) in right branchial chamber, Coco Beach, Puerto Galera, 13°31′32″ N, 120°57′44″ E, coll. J.D. Williams, 14 January 1999 (indicated as 12 January 1999 in Williams et al. 2019). Female (15.2 mm) and male (no measurement) ( ZRC 2022.0962), infesting C. gaimardii (4.4 mm SL), inhabiting unknown shell, Lalaguna Beach, Puerto Galera, 13°31′32″ N, 120°58′8″ E, coll. J.D. Williams, 17 June 2000. Female (4.6 mm) and male (1.5 mm) ( ZRC 2016.0411) from male Pagurojacquesia polymorpha (2.3 mm), inhabiting unknown shell, west off Panglao Island, Station CP2334, 09°37.5′00″ N, 123°40.2′00″ E (see de Forges et al., 2009), beam trawl, 631–659 m, sandy bottom, Panglao Expedition 2005, 22 May 2005.

Hosts: Calcinus gaimardii , Calcinus minutus , Calcinus pulcher , Diogenes senex (type host of Diogenion vermifactus ), Pagurojacquesia polymorpha .

Description of female: Female in abdomen of host surrounded by host induced sheath; positioned with anterior end at posterior end of host and ventral surface of parasite directed to dorsal surface of host (fig. 3A, B). Host tube with exit pore near first pereopod of host (fig. 3B). Head bilobed, with elongated oval lobes (figs. 3C, 4A). Antennulae fused into large, flattened, pad-like structure. Antennae as thin digitate extensions (fig. 4A). Maxillipeds small, round (fig. 4A). Pereon without ovarian processes. Oostegites 1–7 present, progressively smaller posteriorly; oostegite 1 normally folded back posterior to head and surrounded by other oostegites (fig. 3A, B), large and flap-like with rounded anterior end and inner surface lined with pleat-like folds (fig. 3C). Pereopods 1–7 present; pereopods segmented, each with small dactylus present on distal end; scales present (fig. 4B, C). Pleon slender, with five pleomeres; small heart in pleomere 1; pleopods, pleural lamellae and uropods absent (fig. 4D). Brood development synchronous; all larvae at same stage of development.

Description of male: Male found within brood chamber of female. Only one male accompanying female (when present). Body curved ventrally, pale in color with few spots of pigmentation (fig. 4E, F). Head small and rounded. Pair of elongated conical antennulae extending beyond margin of head, terminally setose; pair of conical antennae slightly larger than antennulae each with tuft of terminal setae (fig. 4G). Oral cone with mandibles and maxilliped present (fig. 4G). Seven pereomeres; pereon maximal width at pereomeres 4–6, gradually tapering anteriorly and posteriorly (fig. 4E, F). Six pairs of pereopods present, absent on pereomere 7 (fig. 4F); pereopods multi-segmented, subequal in size, each with curved dactylus (fig. 4H); patch of scales on propodus at point where dactylus terminates on all pereopods (fig. 4H). Pleon of five segments plus pleotelson; pleomeres gradually decreasing in size posteriorly; without appendages (fig. 4E, F). Uropods well developed; terminal setae present (fig. 4E).

Description of epicaridium larva (undergoing molt): Approximately 340 µm in length. Body teardrop shaped and dorsally convex; anterior margin of head rounded (fig. 5A). Head with pair of conical antennulae (segmentation and setae not distinct due to molting process) (fig. 5A, C); pair of long antennae of seven segments, four peduncular and three flagellar, half of total body length when fully extended (fig. 5A, B). Oral cone with pair of maxillipeds on each side of mouth on ventral side. Pereon of seven segments. Six pereopods; subequal in length, subchelate with ovate propodi and curved dactyli (fig. 5A, B). Pleon with five pairs of biramous pleopods, subequal in size, with three short setae on exopod and two short setae on endopod (fig. 5D). Telson tapered to point. Uropods with pointed endopod, slightly longer than exopod, both bearing short terminal setae (fig. 5E).

Remarks: All specimens match the original morphological description of Diogenion vermifactus ( Codreanu et al. 1960) , previously known only infesting Diogenes senex in the Red Sea (fig. 2). However, in this study D. cf. vermifactus was found to parasitize three species of shallow subtidal calcinid hermit crabs, C. gaimardii , C. minutus and C. pulcher and the deeper water pagurid P. polymorpha in the coastal waters of the Philippines, over 8,000 km away from the type locality in the Red Sea (fig. 1). Currently, we cannot morphologically distinguish the Philippine specimens of Diogenion from those of the Red Sea; however, given this disjunct distribution and the barriered nature of the Red Sea ( DiBattista et al. 2016; Schnurr et al. 2018; Hadfield & Smit 2020) it is possible that the Philippine entoniscid is a distinct species from D. vermifactus . Additional data, ideally including molecular sequencing, is needed to clarify whether D. vermifactus is widely distributed across the Indo-West Pacific or represents a species complex ( Hadfield & Smit 2020). At present, the substantial geographic distance between the two localities and diversity of hosts suggests that a designation of “cf.” for the Philippine specimens is warranted pending discovery of additional specimens from along the range.

Many features of the adult Diogenion vermifactus are considered primitive when compared to other members of Entoniscidae ( Codreanu et al. 1960; Adkison 1990). Specifically, the female has segmented pereopods, a brood pouch formed by overlapping oostegites and a synchronously developing brood; males also retain segmented pereopods and possess both pairs of antennae as well as uropods. For these reasons, Adkison (1990) suggested that the genus be placed in its own subfamily. The epicaridium larval stage of D. vermifactus was not previously described except for mention of the narrowness of the larvae, the great length of the appendages and the uniform structure of the pereopods and pleopods ( Codreanu et al. 1960; Adkison 1990). Although previous authors did not provide drawings or detailed descriptions of this larval stage, the present specimens exhibit the gross morphological details reported previously. The present study confirms that the epicaridium larvae have nearly uniform pereopods, i.e., the sixth pereopod is not greatly modified as in the larvae of some entoniscid genera (e.g., Cancrion Giard & Bonnier, 1887 ). However, the epicaridium larvae examined were undergoing a molt, making some features difficult to distinguish, as has been shown to occur in other epicarideans (see Williams & Boyko 2021).

Figures

FIGURE 3. Diogenion cf. vermifactus Codreanu, Codreanu & Pike, 1960, female (A, B = USNM 1522331, C = USNM 1522333). A. Host Calcinus gaimardii with ovigerous female of D. cf. vermifactus partially dissected from abdomen of host, lateral view. B. Same specimen shown in A, dorsal view of host and opposite side of ovigerous female of D. cf. vermifactus showing abdomen extending to exit pore near anterior end of hermit crab (indicated by arrow). C. Ovigerous female of D. cf. vermifactus with nearly all eggs removed, ventral view. Abbreviations: Hd, head; O1, oostegite 1. Scale bars: A, B, C = 3 mm.

FIGURE 4. Diogenion cf. vermifactus Codreanu, Codreanu & Pike, 1960, female (A, B, C = USNM 1522333, D = ZRC 2022.0962), A. Head, ventral view. B. Pereopod 1. C. Pereopod 6. D. Pleon. Male (E= USNM 1522332, F, G, H = USNM 1522334), E. Oblique lateral view. F. Dorsal view. G. Lateral view of head region showing antennula, antenna, pereopod 1 and mouth parts (dashed lines show head region in relation to rest of body). H. Pereopod 6. Abbreviations: A1, antennulae; A2, antennae; Md, mandible; Mxp, maxilliped; P1–P7, pereopods 1–7; Pl1–5, pleomeres 1–5; Pt, pleotelson. Scale bars: A, D = 1.0 mm; B, C = 250 µm; E, F = 500 µm; G, H = 50 µm.

FIGURE 5. Diogenion cf. vermifactus Codreanu, Codreanu & Pike, 1960, epicaridium larvae (USNM 1522332). A. Ventral view. B. Pereopods 1–6. C. Dorsal view. D. Pleopods 1–5, endopod below numbered appendages. E. Dorsal view of pleopods, uropods, and pleotelson. Abbreviations: A1, antennulae; A2, antennae; P1–P6, pereopods 1–6; Pl1–5, pleomeres 1–5; Pt, pleotelson; Ur, Uropod. Scale bars: A, B = 50 μm; C = 100 μm; D, E = 25 μm.