Carcinione platypleura, BOURDON, 1983

Boyko, Christopher B. & Van Der Meij, Sancia E. T., 2018, A trifecta of Swiftian symbioses: stony corals, gall crabs and their parasites (Scleractinia; Brachyura: Cryptochiridae; Isopoda: Epicaridea and Cirripedia: Rhizocephala), Zoological Journal of the Linnean Society 184, pp. 304-329 : 305-310

CARCINIONE PLATYPLEURA BOURDON, 1983

( FIGS 1, 2, 10)

‘ Seventeen specimens of epicarids … collected from four genera of crabs (including Pseudohapalocarcinus )’ Monod & Serène, 1976: 24 (in part) [ex Pseudohapalocarcinus ransoni Fize & Serène, 1956a , Indonesia, examined in this study].

? ‘bopyrid parasites’ Takeda & Tamura, 1980: 54–55 59, pl. 5 [ex P. ransoni Fize & Serène, 1956a , Ryukyu Islands, Japan].

Carcinione platypleura Bourdon, 1983: 854–855 , fig. 6 [ex P. ransoni Fize & Serène, 1956a , Banda Neira, Indonesia, examined in the present study]. – van der Meij, 2014: 45 [ex Opecarcinus cathyae van der Meij, 2014 , Halmahera, Indonesia, examined in this study]. – van der Meij, 2015: fig. 7B [ex Fungicola syzygia van der Meij, 2015 , Bunaken Island, Indonesia, examined in the present study]. – van der Meij, Reijnen & Reimer, 2017: fig. 1F [ex Lithoscaptus sp. , Odo Beach, Okinawa, Japan, examined in the present study].

‘bopyrid isopod’ Kropp, 1994: 534 [ex P. ransoni Fize & Serène, 1956a , Banda Neira, Moluccas, examined in the present study].

‘unidentified bopyrid’ Williams & Boyko, 2012: fig. 1G [ex Lithoscaptus helleri ( Fize & Serène, 1957) , Indonesia, examined in the present study].

Type material

Indonesia: Mature female holotype (2.0 mm) [MNHN-IU-2007-3670 (= MNHN-EP 336)] and cryptoniscus paratype (0.6 mm) [MNHN-IU-2017-8 (= MNHN-Ep 336)], ex female P. ransoni Fize & Serène, 1956a (3.3 mm long × 3.4 mm wide) (MNHN-IU-2016–10934), parasites under right branchiostegite, ex Pavona cactus ( Forskål, 1775) ( Agariciidae ), Banda Neira, Amboine (= Ambon), 29 January 1975, collected by Rumphius II (R. Serène & T. Monod) [crab and coral originally identified by R. Serène, with the coral only identified to genus; crab identification confirmed and coral identified to species by S. E. T. van der Meij).

Additional material

Indonesia: Immature female (1.5 mm) (MNHN-IU-2017-9), ex right branchiostegite of male P. ransoni Fize & Serène, 1956a (2.4 mm long × 2.3 mm wide) (MNHN-IU-2009-5734 [= MNHN-B12674]), ex Pavona cactus ( Forskål, 1775) ( Agariciidae ), southwest corner of Naira Island, at southern entrance to channel between Gunung Api Island and Naira Island, coral, Amboine (= Ambon), 29 January 1975, collected by Rumphius II [this specimen is not part of the type series, although it was collected at the same time, in the same place, and from the same host species as the holotype, but it was not mentioned in the original description by Bourdon (1983)]; mature non-ovigerous female (1.8 mm) and mature male (0.5 mm) (RMNH. Crus.I.7719), ex left branchiostegite, mature ovigerous female (1.7 mm), mature male (0.7 mm) (RMNH. Crus.I.7720), ex right branchiostegite, ex juvenile female Dacryomaia japonica ( Takeda & Tamura, 1981) (2.7 mm long × 2.0 mm wide) (RMNH.Crus.D.54193), ex Leptastrea cf. transversa Klunzinger, 1879 ( Scleractinia incertae sedis), Teluk Makawide Reef, Lembeh Strait, 01°29′05″N, 125°14′26″E, 9 February 2012, coll. S. E. T. van der Meij; mature non-ovigerous female (3.3 mm) and mature male (0.9 mm) (RMNH. Crus.I.7721), ex right branchiostegite of mature non-ovigerous female F. syzygia van der Meij, 2015 (5.0 mm long × 4.3 mm wide) (RMNH.Crus.D.53224), ex Pleuractis granulosa ( Klunzinger, 1879) ( Fungiidae ), Tanjung Pasir Putih Reef, Ternate, 00°51′50″N, 127°20′37″E, 2 November 2009, coll. S. E.T.van der Meij; mature ovigerous female, non-ovigerous (3.6 mm) and mature male (1.1 mm) (RMNH.Crus.I.7722), ex right branchiostegite, cryptoniscus larva (0.6 mm) (RMNH. Crus.I.7723), ex left branchiostegite, ex mature non-ovigerous female F. syzygia van der Meij, 2015 (4.3 mm long × 3.7 mm wide) (RMNH.Crus.D.56481), ex Pleuractis paumotensis ( Stutchbury, 1833) ( Fungiidae ), Alung Banua Reef, Bunaken Island, 01°37′07″N, 124°45′30″E, 19 December 2008, coll. S. E. T. van der Meij; mature non-ovigerous female (2.3 mm) (RMNH. Crus.I.7724), ex right branchiostegite of male F. syzygia van der Meij, 2015 (3.3 mm long × 3.2 mm wide) (RMNH.Crus.D.56482), ex Pleuractis paumotensis ( Stutchbury, 1833) ( Fungiidae ), Siladen I Reef, Siladen Island, 01°37′31″N, 124°47′54″E, 18 December 2008, coll. S. E. T. van der Meij; mature ovigerous female (3.6 mm), mature male (1.3 mm) (RMNH.Crus.I.7725), ex right branchiostegite of male Lithoscaptus prionotus Kropp, 1994 (5.3 mm long × 3.5 mm wide) (RMNH. Crus.D.54171), ex Oulophyllia crispa (Lamarck, 1816) ( Merulinidae ), Tanjung Kuning Reef, Lembeh Strait, 01°23′10″N, 125°10′23″E, 11 February 2012, coll. S. E. T. van der Meij; mature ovigerous female (4.3 mm), mature male (1.5 mm) (RMNH.Crus.I.7726), ex left branchiostegite of non-ovigerous female L. helleri ( Fize & Serène, 1957) (5.7 mm long × 4.2 mm wide) (RMNH. Crus.D.54057), ex Favites cf. complanata ( Ehrenberg, 1834) ( Merulinidae ), Siladen I Reef, Siladen Island, 01°37′31″N, 124°47′54″E, 18 December 2008, coll. S. E. T. van der Meij; mature ovigerous female (2.5 mm), mature male (1.0 mm), cryptoniscus larva (0.7 mm) (RMNH.Crus.I.7727), ex right branchiostegite of male L. helleri ( Fize & Serène, 1957) (3.5 mm long × 2.6 mm wide) (RMNH. Crus. D.56121), ex Favites cf. complanata ( Ehrenberg, 1834) ( Merulinidae ), Lekuan I Reef, Bunaken Island, 01°35′44″N, 124°46′12″E, 11 December 2008, coll. S. E. T. van der Meij; mature ovigerous female (2.2 mm), mature male (0.9 mm) (RMNH.Crus.I.7728), ex right branchiostegite of male Lithoscaptus cf. bani ( Fize & Serène, 1957) (telson abnormally wide) (3.2 mm long × 2.3 mm wide) (RMNH. Crus.D.56121), ex Goniastrea pectinata ( Ehrenberg, 1834) ( Merulinidae ), Negiri Reef, Manado Tua Island, 01°36′58″N, 124°41′39″E, 5 December 2008, coll. S. E. T. van der Meij; mature ovigerous female (3.3 mm), mature male (0.9 mm) (RMNH.Crus.I.7729), ex right branchiostegite of non-ovigerous female Lithoscaptus sp. 1 (A) (4.3 mm long × 2.9 mm wide) (RMNH.D.54067), ex Astrea curta Dana, 1846 ( Merulinidae ), Ron’s Point, Bunaken Island, 01°36′21″N, 124°44′13″E, 9 December 2008, coll. S. E.T. van der Meij; mature ovigerous female (3.1 mm), mature male (1.3 mm) (RMNH.Crus.I.7730), ex right branchiostegite, mature ovigerous female (3.1 mm), mature male (1.1 mm) (RMNH.Crus.I.7731), ex left branchiostegite of non-ovigerous female Lithoscaptus sp. 2 (B) (4.0 mm long × 3.3 mm wide) (RMNH.Crus.D.54106), ex Plesiastrea versipora (Lamarck, 1816) ( Scleractinia incertae sedis), Lekuan III, Bunaken Island, 01°36′20″N, 124°46′08″E, 12 December 2008, coll. S. E. T. van der Meij; mature ovigerous female (2.7 mm), mature male (1.0 mm) (RMNH.Crus.I.7732), ex left branchiostegite of juvenile female Lithoscaptus sp. 2 (B) (4.0 mm long × 2.5 mm wide) (RMNH.Crus.D.54172), ex P. versipora (Lamarck, 1816) ( Scleractinia incertae sedis), Pulau Abadi, Lembeh Strait, 01°26′01″N, 125°12′22″E, 10 February 2012, coll. S. E. T. van der Meij; cryptoniscus larvae (0.6 mm) (RMNH. Crus.I.7733), ex dorsal carapace of feminized male Opecarcinus sp. 1 (F) (3.0 mm long × 2.3 mm wide) (RMNH.Crus.D.53990; host also parasitized by one Sacculina quadrialata sp. nov., RMNH.Crus.C.10249), ex Leptoseris mycetoseroides Wells, 1954 ( Agariciidae ), South Pilongga, Tidore, 00°42′44″N, 127°28′47″E, 12 November 2009, coll. S. E. T. van der Meij; mature ovigerous female (4.0 mm), mature male (1.5 mm) (RMNH.Crus.I.7734), ex right branchiostegite of non-ovigerous female Opecarcinus pholeter Kropp, 1989 (5.3 mm long × 4.3 mm wide) (RMNH.Crus.D.54000), ex Pavona explanulata (Lamarck, 1816) ( Agariciidae ), Sulamadaha II, Ternate, 00°52′02″N, 127°19′46 ″E, 6 November 2009, coll. S. E. T. van der Meij; immature female (1.8 mm), mature male (0.8 mm) (RMNH. Crus.I.7735), ex right branchiostegite, immature female (1.5 mm), mature male (0.7 mm) (RMNH.Crus.I.7736), ex left branchiostegite of male O. pholeter Kropp, 1989 (3.3 mm long × 2.7 mm wide) (RMNH.Crus.D.54000), ex P. explanulata (Lamarck, 1816) ( Agariciidae ), Sulamadaha II, Ternate, 00°52′02″N, 127°19′46″E, 6 November 2009, coll. S. E. T. van der Meij; mature ovigerous female (2.8 mm), mature male (1.2 mm) (RMNH.Crus.I.7737), ex right branchiostegite of male Opecarcinus cathyae van der Meij, 2014 (4.0 mm long × 2.7 mm wide) (RMNH.Crus.D.53923), ex Pavona clavus (Dana, 1846) ( Agariciidae ), South Lela, Gura Ici, 00°01′51″S, 127°15′03″E, 10 November 2009, coll. S. E. T. van der Meij; mature non-ovigerous female (1.5 mm), ex right brachiostegite, mature non-ovigerous female (1.5 mm), ex left brachiostegite, mature male (0.8 mm), ex unknown brachiostegite (RMNH. Crus.I.7738), ex juvenile female Xynomaia sheni ( Fize & Serène, 1956b) (2.7 mm long × 1.8 mm wide) (RMNH.Crus.D.54115), ex Mycedium elephantotus ( Pallas, 1766) ( Merulinidae ), Lobangbatu Besar, Lembeh Strait, 01°25′49″N, 125°11′26″E, 7 February 2012, coll. S. E. T. van der Meij; mature ovigerous female (2.4 mm), mature male (1.2 mm) (RMNH. Crus.I.7739), ex right branchiostegite of male X. sheni ( Fize & Serène, 1956b) (4.0 mm long × 2.7 mm wide) (RMNH.Crus.D.54085), ex Pectinia sp. ( Merulinidae ), Mandolin, Bunaken Island, 01°36′44″N, 124°43′57″E, 9 December 2008, coll. S. E. T. van der Meij.

Malaysia: Mature ovigerous female (5.0 mm), mature male (1.5 mm) (RMNH.Crus.I.7740), ex left branchiostegite of non-ovigerous female L. prionotus Kropp, 1994 (7.1 mm long × 5.2 mm wide) (RMNH. Crus.D.53719), ex Oulophyllia crispa (Lamarck, 1816) ( Merulinidae ), Erzherzog Reef, Semporna, Malaysia, 04°14′26″N, 118°23′35″E, 1 December 2010, coll. S. E. T. van der Meij.

Maldives: Immature female (1.7 mm) ex right branchiostegite, immature female (1.6 mm) ex left branchiostegite (RMNH.Crus.I.7700), ex female F. syzygia van der Meij, 2015 (3.3 mm long × 3.1 mm wide) (RMNH.Crus.D.57063), ex P. granulosa ( Klunzinger, 1879) ( Fungiidae ), Sunny Reef, Faafu Atoll, 03°08′40″N, 73°00′45″E, 19 February 2015, coll. S. E. T. van der Meij; mature non-ovigerous female (1.5 mm), mature male (0.7 mm) (RMNH.Crus.I.7701), ex left branchiostegite of female Opecarcinus sp. (2.0 mm long × 1.7 mm wide) (RMNH.Crus.D.57064), ex L. mycetoseroides Wells, 1954 ( Agariciidae ), Wallino, Faafu Atoll, 03°05′12″N, 72°57′23″E, 21 February 2015, coll. S. E. T. van der Meij; mature female with brood of epicaridean larvae (3.3 mm), mature male (1.1 mm) ex right branchiostegite, mature non-ovigerous female (3.1 mm), mature male (1.2 mm) (RMNH.Crus.I.7704) ex left branchiostegite of female Lithoscaptus sp. Z (5.4 mm long × 3.7 mm wide) (RMNH.Crus.D.57066); immature female (1.1 mm), mature male (0.9 mm) (RMNH.Crus.I.7704) ex right branchiostegite of male Lithoscaptus sp. Z (RMNH. Crus.D.57066), ex Dipsastraea cf. vietnamensis ( Veron, 2000) ( Merulinidae ), Wallino, Faafu Atoll, 03°05′13″N, 72°57′24″E, 26 February 2015, coll. S. E. T. van der Meij; mature ovigerous female (1.5 mm), mature male (0.8 mm) (RMNH.Crus.I.7703), ex left branchiostegite of male Lithoscaptus sp. Z (3.6 mm long × 2.3 mm wide) (RMNH.Crus.D.57066), ex D. cf. vietnamensis ( Veron, 2000) ( Merulinidae ), Wallino, Faafu Atoll, 03°05′13″N, 72°57′24″E, 26 February 2015, coll. S. E. T. van der Meij; mature ovigerous female (3.3 mm), mature male (1.4 mm) (RMNH.Crus.I.7702), ex left branchiostegite of female Lithoscaptus sp. (5.2 mm long × 3.0 mm wide) (RMNH.Crus.D.57065), ex Favites aff. flexuosa (Dana, 1846) ( Merulinidae ), Beyrufushi, Faafu Atoll, 03°06′29″N, 73°01′07″E, 26 February 2015, coll. S. E. T. van der Meij.

Japan: Immature female (1.1 mm) (RMNH. Crus.I.7741), ex right branchial chamber of male Dacryomaia sp. (2.3 mm long × 1.5 mm wide) (RMNH. Crus.D.57231), ex Leptastrea sp. ( Scleractinia incertae sedis), Red Beach, Okinawa, 26°26′47″N, 127°54′43″E, 14 April 2016, coll. S. E. T. van der Meij; mature female (3.5 mm) (RMNH.Crus.I.7742) with immature female Cabirops (2.1 mm) and cryptoniscus larva (1.3 mm) (RMNH.Crus.I.7743) in marsupium, immature male (1.7 mm), ex right branchial chamber of female Lithoscaptus sp. (5.2 mm long × 3.8 mm wide) (RMNH.Crus.D.57232), ex Coelastrea aspera (Verrill, 1866) ( Merulinidae ), Odo Beach, Okinawa, 26°05′22″N, 127°42′33″E, 22 April 2016, coll. S. E. T. van der Meij; ovigerous female (2.6 mm) (RMNH.Crus.I.7744) with three associated Cabirops cryptoniscus larvae (1.2, 1.2, 1.3 mm) (RMNH.Crus.I.7745–7746), mature male (1.1 mm), (RMNH.Crus.I.7747), ex right branchial chamber, mature female (2.9 mm) with ovigerous Cabirops female (2.9 mm long × 1.5 mm wide) and cryptoniscus larva (1.0 mm) (RMNH.Crus.I.7748) in brood chamber, mature male (1.0 mm), ex left branchial chamber of male Xynomaia sp. (4.3 mm long × 3.8 mm wide) (RMNH.Crus.D.57233), ex Pectinia sp. ( Merulinidae ), Blue Tombs, Henza Island, Okinawa, 26°21′46″N, 127°59′50″E, 29 April 2016, coll. S. E. T. van der Meij.

Redescription

Female ( Fig. 1): Body length 4.3 mm, maximal width 2.3 mm, head length 0.9 mm, head width 0.9 mm. Pereon nearly straight, head not deflected ( Fig. 1A, B). All body regions and pereomeres distinctly segmented.

Head subrectangular, approximately as broad as long, usually overlapping entire first pereomere medially ( Fig. 1A), but sometimes only overlapping in part Fig. 1C), with moderately broad frontal lamina ( Fig. 1A, C). Eyes minute, distolaterally placed. Antennule of four articles; antenna of two articles ( Fig. 1D). First oostegite ( Fig. 1E) anterior lobe globular, posterior lobe slightly smaller than anterior lobe, ovate with rounded margins, distal projection lacking but with medially directed smooth lobe, internal ridge thick, smooth. Oostegites completely enclosing the marsupium. Maxilliped ( Fig. 1F) with short, rounded fleshy spur; palp lacking, anterior segment triangular, rounded, posterior segment irregularly subquadrate. Barbula smooth ( Fig. 1G).

Pereon composed of seven pereomeres ( Fig. 1A, C), broadest across pereomeres III–V, only slightly tapering anteriorly and posteriorly; pereomere I posterior margin usually under head, II anteromedially concave, III weakly anteromedially concave to weakly convex, IV anteromedially straight to weakly convex, V–VII weakly convex. Coxal plates very reduced, largest on pereomeres I, II, large dorsolateral bosses on pereomeres I–IV or I–V (those on V sometimes much smaller than other pairs). Anterior pereopods ( Fig. 1H) much smaller than posterior pairs ( Fig. 1I), posterior pairs about two times as large.

Five pleomeres plus pleotelson ( Fig. 1A, C), lateral plates well developed, edges crenulated, those on pereopods I–III about twice as broad as other pairs ( Figs 1A–C, 2A). Pleomere I with biramous pleopods, II–V with uniramous pleopods all subequal in size, uniramous uropods resembling lateral plates, edges crenulated ( Fig. 2A).

Male ( Fig. 2B): Length 1.5 mm, maximal width 0.5 mm, head length 0.2 mm, head width 0.3 mm, pleon length 0.5 mm.

Head ovate, widest posteriorly, distinct from first segment of pereon ( Fig. 2B); eyes present posterolaterally. Antennule of four articles ( Fig. 2D), distally setose, not extending beyond margin of head; antenna of three articles, terminal article less than half as large as second segment, distally setose ( Fig. 2D).

Pereomere III–V broadest, others gradually tapering anteriorly and posteriorly. All pereomeres slightly concave anteriorly, convex posteriorly, distal margins rounded. All pereopods ( Fig. 2C) subequal, all articles distinctly separated.

Pleon with five segments plus pleotelson. All pleomeres directed laterally ( Fig. 2B, C), with distolateral margins rounded. Midventral tubercles, pleopods and uropods lacking; small anal cone mediodistally on pleotelson ( Fig. 2C).

Remarks

Bourdon (1983) described this species on the basis of the single female mentioned obliquely by Monod & Serène (1976); although he had a cryptoniscus larva, he did not describe it. The male has not been described previously. The characters of the female, particularly the wide anterior lateral plates, made Bourdon (1983) unsure of the subfamily in which to place this species. He indicated that he did not think it belonged to the ‘Céponiens’ (now Keponinae ), but that the female somewhat resembled those of Pseudioninae . Given the lack of female characters that clearly placed this genus in any particular subfamily, Boyko et al. (2013) somewhat arbitrarily placed the genus with the other brachy-uran parasites in Keponinae . However, the discovery of the male provides characters that are very similar to those of most males in Pseudioninae and not at all like males belonging to Keponinae . Therefore, Carcinione is here placed with confidence in Pseudioninae .

This species appears to be the most common parasite of gall crabs, with a wide distribution in the Indo-West Pacific. The fact that it was described from only a single mature female and a cryptoniscus larva and has subsequently been reported only once before the present study ( Sanabe & Tsuchiya, 2005) is explained by limited sampling of hosts rather than genuine scarcity of the parasites. This conclusion is supported by the data of Sanabe & Tsuchiya (2005), where 10.64% of P. ransoni (N = 357) collected in the Ryukyus, Japan, were infested with a bopyrid identified as C. platypleura . Although we have not seen any of Sanabe & Tsuchiya’s specimens, we are confident in their identification of the bopyrid species.

The parasitized Xynomaia sp. from Okinawa might well hold the record for the most parasites and hyperparasites associated with a single host. This male crab has an ovigerous female C. platypleura with a mature male in the right branchial chamber and a mature, non-ovigerous C. platypleura in the left branchial chamber. The bopyrid in the right chamber, despite being ovigerous, co-occurs with three Cabirops cryptoniscus larvae, one of which is in the marsupium amongst the eggs. The bopyrid in the left branchian chamber contains an ovigerous Cabirops in the marsupium and a cryptoniscus larva. As if this were not enough energy burden on the host, there is an immature female bopyrid (RMNH.Crus.I.7750) under the abdomen, which belongs to a new bopyrid genus and species described in the next subsection. This single host, therefore, has an astounding five bopyrid parasites, belonging to two species, and five hyperparasitic cryptoniscoids associated with it. The Cabirops species, being hyperparasitic and found associated with C. platypleura from two hosts in Okinawa, will be described in a future paper.

Known hosts

Dacryomaia japonica ( Takeda & Tamura, 1981) , Dacryomaia sp. , F. syzygia van der Meij, 2015 , L i t h o s c a p t u s c f. b a n i (F i z e & S e r è n e, 1 9 5 7), L. helleri ( Fize & Serène, 1957) , L. prionotus Kropp, 1994 , Lithoscaptus sp. , Lithoscaptus sp. 1 (A), Lithoscaptus sp. 2 (B), Lithoscaptus sp. Z, Opecarcinus cathyae van der Meij, 2014 , Opecarcinus pholeter Kropp, 1989 , Opecarcinus sp. 1 (F), P. ransoni Fize & Serène, 1956a , X. sheni ( Fize & Serène, 1956b) , Xynomaia sp.

Distribution

Known from localities in Indonesia, Malaysia, Maldives and Japan.