Ione thoracica ( Montagu, 1808 )

Boyko, Christopher B., Williams, Jason D. & Shields, Jeffrey D., 2017, Parasites (Isopoda: Epicaridea and Nematoda) from ghost and mud shrimp (Decapoda: Axiidea and Gebiidea) with descriptions of a new genus and a new species of bopyrid isopod and clarification of Pseudione Kossmann, 1881, Zootaxa 4365 (3), pp. 251-301 : 256-259

Ione thoracica ( Montagu, 1808)

Figs 1D , 2

Oniscus thoracicus Montagu, 1808: 103 –104, pl. 3, figs. 3–4 (type locality: Devonshire, England, infesting Cancer subterraneus = Callianassa subterranea (Montagu, 1808)) .— Leach, 1813 –1814: 405–406 (description of Montagu, 1808, repeated).— Latreille, 1817: 54 (list).— Duvernoy, 1841: 113 (mention).

Oniscus (Ione) thoracicus — Latreille, 1818: pl. 336, fig. 46.

Ione thoracica — Lamarck, 1818: 170 –171 (list).— Guérin-Méneville, 1836: 22 (list), pl. 26, figs. 1–2.— White, 1857: xi (figure caption), 254–255, pl. 14, fig. 8a–b.— McAndrew, 1861: 225 (list).—Bate & Westwood, 1867: 255–256 (discussion), unnumbered fig. (copied from H. Milne Edwards, 1840).— Carus, 1885: 453 (list).— Giard & Bonnier, 1886: 890 (mention).— Norman, 1886: 13 (list).— Giard & Bonnier, 1887a: 23, 29, 36, 63, 76–77 (list), fig. 6.II. —Giard, 1887: 1115 (mention).— Giard & Bonnier, 1887b: 1309 (mention).— Groult, 1887: 165 –166 (brief discussion), pl. 11, fig. 13.—Giard, 1888: 28 (mention).— Lo Bianco, 1888: 410 (list).— Giard & Bonnier, 1889: 259 (mention).— Giard & Bonnier, 1890b: 376, 377, 381, 385, 387, 388 (discussion, list).— Ide, 1892: 100, 148, 149, pl. 7, figs. 95–97 (structure of male and female digestive tracts).— Perrier, 1893: 1021 (list).— Bonnier, 1900: 8, 152, 164, 166–167, 238–245, 247, 273, 381, pls. 1, 2, 3, figs. 1–6, text fig. 43.— Richard, 1900: 71 (list).— Gerstaecker & Ortmann, 1901: 153 (mention), 156–157 (mention), 185 (list), 254, 256–258 (list).— Richardson, 1904: 78 (mention).— Norman, 1905a: 17 (list).— Norman, 1905b: 86, 93 (list).— Norman & Scott, 1906: vii, 52 (list).— Sinel, 1906: 224 (list).— Norman, 1907: 363 (list).— Lo Bianco, 1909: 594, 603 (list).— Giard, 1913: 408, 419 (mention).— Guiart, 1913: 3 (list).—Nierstrasz & Brender à Brandis, 1923: 80 (mention).— Caroli, 1928: 321 –326 (larval development).— Caroli, 1929b: 501 (mention).— Popov, 1929: 6, 10, 11, 17, 25 (occurrence in Kilen Bay on C. subterranea ).— Tucker, 1930: 7 –8 (mention).— Caroli, 1931: 316, 319, 320 (mention).— Schmitt 1931: 159, fig. 31 (figure after Bonnier, 1900).— Tattersall, 1931: 187 (list).— Caspers, 1939: 243 (list).— Reverberi, 1941: 187, 197, figs. 3, 4 (Naples, infesting Callianassa laticauda Otto, 1828 = Pestarella tyrrhena (Petagna, 1792)) .— Reverberi, 1942b: 91 –93, 98, 99 (Naples, infesting C. laticauda = P. tyrrhena ).— Carayon, 1943: 47 (mention).—Reverberi & Pitotti, 1943: 111–184 (biology, development), figs. 1–27.— Reverberi, 1943a: 2, 42, 48, 72, 76, 94, 96, 101 (mention).— Reverberi, 1943b: 231, 233, 277–289, 296–298, 303, 309, 311, table 18–29, 42 (effects on C. laticauda = P. tyrrhena ).— Reverberi, 1945: 227, 230, 237–240, fig. 7 (development; effects on P. tyrrhena ).— Veillet, 1945: 297 (mention).— Reverberi, 1947b: 81 –85, 87, 90, 91 (Naples, infesting C. laticauda = P. tyrrhena and Upogebia littorialis (Risso, 1816) = U. pusilla (Petagna, 1792) (experimental infestation)).— Baffoni, 1948: 134 (mention).— Baffoni, 1950: 213, 216. 218– 222 (Naples, infesting C. laticauda = P. tyrrhena ).— Holthuis, 1950: 15 (North Sea on C. subterranea ).— Caullery, 1952: 70, 75–76 (discussion of sex change).— Reverberi, 1952: 292 (mention).— Baffoni, 1953: 438 –442 ( Italy, infesting C. laticauda = P. tyrrhena ).— Pike, 1953: 235 (occurrence at Jersey, England on C. stebbingi = P. tyrrhena ).— Attardo, 1955: 125 (mention).— Reinhard, 1956: 89, 90, 101 (effects on hosts).— Spooner, 1957: 205 (list).— Charniaux-Cotton, 1960: 434 –435 (mention).— Tuzet et al., 1960: 505 (mention).— Holme, 1961: 453 (list).— Holme, 1966: 475 (list), 490, fig. 53 (distribution).— Bourdon, 1964: 3 (list).— Noble & Noble, 1964: 561 (mention).— Shiino, 1964a: 30 (mention).— Schmitt, 1965: 96, fig. 39 (figure after Bonnier, 1900).— Cals, 1966: 132 (mention).— Codreanu, 1967: 204 (mention).— Bourdon, 1968: 82 –94, fig. 1–8, 9b (synonymy list, redescription, biological data), 95 (comparison with I. vicina ), 121, 124, 128, 133, 134, 147, 157, 217, 408 (synonymy of I. gebiae ), 410.— Field, 1969: 1273 (discussion of larvae).— Sadoğlu, 1969: 175, 194–196, 201, 203, 206, figs. 17, 18, 20, 23B, 25B (eye development).— Danforth, 1970b: 19, 20 (mention).— Kaestner, 1970: 425 (mention).— Noble & Noble, 1971: 475 (mention).— Rioja, 1971: 511 (mention).— Bourdon, 1972: 101 (mention).— Naylor, 1972: 69 (list), 73 (characters), fig. 23j–l.— Cheng, 1973: 715 –716 (review of life cycle).— Beck, 1980a: 148 (mention).— Bourdon, 1980: 1, 2 (Roscoff, France, infesting C. tyrrhena = P. tyrhhena ).— Adema, 1981: 61 – 62, fig. 1 ( Netherlands, infesting C. subterranea ).— Anderson & Dale, 1981: 143, 153 (larval host preferences discussed).— Bourdon, 1981b: 120 (mention).—Bourdon et al., 1981: 497, 500 (mention).— Adema & Huwae, 1982: 33, 46–47, fig. 5 (record from Netherlands).— Ross, 1983: 167, table 1 (list).— Anderson & Dale, 1989: 16 (mention).— Müller, 1989: 43 (mention).— Wägele, 1989: 214 –215, fig. 98 (life cycle, phylogeny).— Isaac et al., 1990: 402 –404 (list; species characters), fig. 9.15.— Owens & Rothlisberg, 1991: 785 (mention).— Brandt, 1993: 126 (mention).— Raibaut & Trilles, 1993: 374, 375, 429–431 (review of life cycle), figs. 11c, 50.— Janssen & Brandt, 1994: 9 –11, fig. 1 (review of life cycle).— Legrand & Juchault, 1994: 684 –685 (mention).— Rowden & Jones, 1994: 623, 625, 629, 633, table 4 (prevalence levels on C. subterranea from the North Sea).— Hayward et al. 1995: 358 –360 (list), fig. 8.25.— Markham, 1995: 86 (mention).— Astall et al., 1996: 822 (mention).— Dworschak, 1998: 1536, 1536, 1543, 1545, table 1 (prevalence levels in P. tyrrhena from the Adriatic Sea).— Markham & Boyko, 1999: 3 (mention).— Trilles, 1999: 288, 293, 295, 296, 305, 323, 330, 334, 335, figs. 8.8F, 8.12B, 8.14D, 8.16D.— Mariappan et al., 2000: 305 (mention).— Dreyer & Wägele, 2001: 172, 175, fig. 10 (life cycle).— Markham, 2001: 196 (mention), 197 (in part, not material from Nigeria), 199–201 (list, in part, not material from Nigeria).—Van der Land, 2001: 322 (list).— Torres Jorda & Roccatagliata, 2002: 725 (mention).— Junoy & Castelló, 2003: 303 (list).— Wardiatno, 2004: 83 (mention).— Legrand & Juchault, 2006: 421 (mention).—Román- Contreras, 2008a: 282 (mention).— Meconcelli et al., 2015: 43 (mention).— Subramoniam, 2017: 7 (table), 17 (mention).

Jone [sic] thoracicus — Brébisson, 1825: 254 (brief discussion).— Desmarest, 1825: 286, pl. 46, fig. 10.— Audouin & H. Milne Edwards, 1826: 359 –361, pl. 49, figs. 10–11.—H. Milne Edwards, 1840a: 279 –280 (list).—H. Milne Edwards, 1840b: pl. 59, fig. 1.— Verril, 1869: 243 (mention).— Stalio, 1877: 1386 (240 in separately paginated reprint volume) (list).

Iona [sic] thoracica — Bosc & Desmarest, 1830: 129 (list).— Lamarck, 1838: 293 (list).—H. Milne Edwards, 1840a: pl. 33, figs. 14–15.

Ione thoracique—Bosc & Desmarest, 1830: 129 (list), pl. 15bis, fig. 5.

Ione thoracicus — Lucas, 1840: 246, pl. 19, figs. 2–3.—H. Milne Edwards, 1843: 174 –175 (discussion).— White, 1847: 111 (list).—Van der Hoeven, 1849: 746 (list).— White, 1850 (81 (list).— Gosse, 1855: 133 (list), fig. 227.— Lucas, 1883: LXXVIII–LXXIX (Mediterranean, infesting C. subterranea ).— Stebbing, 1893: 414 (list).— Tattersall, 1905: 86 (list).

Jone [sic] thoracica — Cornalia & Panceri, 1861: 115 –116 (list).— Heller, 1866: 749 –750 (list).— Nardo, 1868: 268 (list).— Fraisse, 1877: 52 (Naples, infesting Gebia littoralis Risso, 1816 = U. pusilla ).— Fraisse, 1878a: 290 (same data as Fraisse, 1877).— Fraisse, 1878b: 405, 417 (mention).— Stossich, 1880: 229 (list).— Kossmann, 1881a: 653, 665, pl. 33, figs. 14–16 (illustration of head appendages).— Kossmann, 1881b: 170 –181, pl. 10, figs. 1–9.— Walz, 1882: 178, 193 (mention).— Gerstaecker & Ortmann, 1901: pl. 11, figs. 1–3.— Giard & Bonnier, 1887a: 176 (mention).— Giard & Bonnier, 1889: 259 (mention).— Giard, 1899: 497 (47 in alternately paginated edition) (list).— Giard, 1913: 129 (list).— Reverberi, 1942a: 58 ( Italy, infesting C. laticauda = P. tyrrhena ).— Reverberi, 1945: 235, 237–239, figs. 6, 8, 9 (development; effects on P. tyrrhena ).— Reverberi, 1947a: 345 –347 (development; effects on C. laticauda = P. tyrrhena ).— Kaestner, 1967: 1161 (mention).— Restivo, 1968: 505 (Naples, infesting C. laticauda = P. tyrrhena ).

Iones [sic] thoracicus — Van Beneden, 1876: 145 (mention).

“a parasite… makes its home within the thoracic plate of the burrowing crab ( Callianassa subterranea )” Wood & Holder, 1885: 478 (mention).

Ione vicina Giard & Bonnier, 1890b: 376 , 385, 387 (nomen nudum) (Naples, infesting Callianassa truncata Giard & Bonnier, 1890 ).— Stebbing, 1893: 414 (list).— Reverberi, 1943a: 42 –43 (mention) (new synonymy).

Ione gebiae Giard & Bonnier, 1890b: 377 , 398 (nomen nudum) (Naples, infesting Gebia stellata = Upogebia stellata ( Montagu, 1808) .— Stebbing, 1893: 414 (list).— Bonnier, 1900: 222, 248 (nomen nudum).— Richard, 1900: 71 (list).—Nierstrasz & Brender à Brandis, 1923: 80 (mention).— Shiino, 1964a: 30, 32 (mention).— Bourdon, 1968: 408 (list).

Ione vicina Bonnier, 1900: 48 , 61, 222, 247–248, 294, pl. 3, figs. 7–15 (type locality: Naples, Italy, infesting C. truncata ).— Richard, 1900: 71 (list).— Richardson, 1905: 505, 507 (mention).—Nierstrasz & Brender à Brandis, 1923: 80 (mention).— Caroli, 1929b: 501 (mention).— Caroli, 1931: 320 –321 (mention).— Caspers, 1939: 243 (list).— Reverberi, 1943b: 233, 297–299, 301, figs. 47, 50, 51 (effects on C. truncata ).— Baffoni, 1949: 237 (mention).— Shiino, 1964a: 30, 32 (mention).— Bourdon, 1968: 82 (mention), 94–95, fig. 9A (after Bonnier, 1900).— Restivo, 1970: 305, 314 (mention).— Argano et al., 1995: 23 (list).— Markham, 1995: 86 (mention).— Abed-Navandi & Dworschak, 1997: 568 (first report from Croatian C. truncata ).— Trilles, 1999: 296, 334 (mention), fig. 8.16C.— Markham, 2001: 199 –200 (list).—Van der Land, 2001: 322 (list) (new synonymy).

Jone [sic]— Reverberi, 1947b: fig. 1 (Naples, infesting C. laticauda = P. tyrrhena ).

Ione — Reveberi, 1947b: figs. 2–7, 9 (Naples, infesting C. laticauda = P. tyrrhena and U. littoralis = U. pusilla [experimental infestation]).

Ione Thoracica — Brezeanu & Elian, 1958: 1181 (mention).

Jone [sic] vicina — Restivo, 1968: 505 (none found at Naples on C. truncata ).

Jone [sic] gebiae — Restivo, 1968: 506, table 3 (none found at Naples on Upogebia littoralis = U. pusilla ).

“a bopyrid parasite” Hughes, 1998: 60–61 (summary of data from Rowden & Jones, 1994).

not Ione thoracica — Olaosebikan, 1986: iv, vi, vii, viii, 9, 27–32, 39, 40, fig. 13 ( Nigeria, infesting Callianassa balssi Monod, 1933 = Callichirus balssi (Monod, 1933)) (= Ione undescribed sp.).

Material examined. Croatia: Mature female (11.8 mm), mature male (4.5 mm) ( NHMW 25382 ), ex branchial chamber of Pestarella tyrrhena (sex and size unknown), Volosko, coll. D. Abed-Navandi , 18 May 2000; mature female (5.5 mm), mature male (2.2 mm) (NHMW 25807), ex branchial chamber of female Callianassa truncata (4.9 mm CL) (NHMW 14779/K6), Kvarner, Volosko, coll. D. Abed-Navandi, 15 Jul 1996; mature female (9.4 mm), mature male (3.3 mm) ( NHMW 25810 ), ex left branchial chamber of male N. truncata (9.0 mm CL) ( NHMW 25014 , Fig. 1D ), Volosko , Croatia, coll. D. Abed-Navandi , Apr 2003. Italy: Mature female (12.0 mm), mature male (5.7 mm) ( NHMW 25231 ), ex branchial chamber of female P. tyrrhena (13.2 mm CL) ( NHMW 25853 ), Lido di Staranzano, coll. P. Dworschak , 11 May 1988; 4 ovigerous females (8.7– 11 mm), 2 mature males (5.1–5.3 mm), 1 partial mature male (posterior end only), ex unknown host, Naples Aquarium , coll. unknown , 17 Nov 1890 (NMV J62892 ). Tunisia: Mature female (4.8 mm), mature male (2.5 mm) ( NHMW 25809 ), ex branchial chamber of male C. truncata (6.4 mm CL) ( NHMW 18819 /7), Hammamet, ca. 2 m, coll. P. Dworschak 15 Jan 2000.

Distribution. Northwestern Atlantic ( Netherlands, Belgium, United Kingdom, France); Mediterranean ( Spain, Tunisia, Italy); Adriatic Sea ( Croatia); and Black Sea.

Hosts. Callianassa subterranea ( Montagu, 1808) (type host), C. truncata Giard & Bonnier, 1890 , and Pestarella tyrrhena (Petagna, 1792) .

Remarks. Bourdon (1968) compared Ione thoracia with I. vicina based on Bonnier’s (1900) data as he did not have any bopyrids from Callinassa truncata available to examine. Bourdon (1968) concluded that the only apparent differences between the two species were in the shapes of the endopods and lateral plates of the first pleopods ( Fig. 2 ). We examined five pairs of Ione from C. truncata and Pestarella tyrrhena , including: three from Croatia ( Figs 1D , 2C, E ), one from Italy ( Fig. 2D ), and one from Tunisia ( Fig. 2F ). Whereas the Croatian females show near identical morphology to the Italian specimen illustrated by Bonnier (1900; repeated by Bourdon 1968: fig. 9 A; Fig. 2 A herein) in the morphology of the first pleopod endopods, lateral plates, and appearance of short endopods ( Fig. 2C, E ), the Tunisian ( Fig. 2F ) and newly examined Italian females ( Fig. 2D ) have first pleopods that are identical to that of the “typical” I. thoracica ( Bourdon 1968: fig. 9B; Fig. 2B herein) in possessing long endopods. The specimen Bonnier (1900) identified as I. thoracica came from an unspecified locality that was most likely Wimereux, France. In other respects the females are essentially identical, as are the males. This leads us to conclude that there is no good reason to maintain I. vicina as distinct from I. thoracica ; therefore, we herein synonymize the two species. Interestingly, specimens occurring on Pestarella tyrrhena from Italy and Croatia both show “typical” I. thoracica morphology for the first pleopod, suggesting there may be a population on C. truncata around Italy and Croatia that show the “ vicina ” morphology of the first pleopod, perhaps due to isolation from other populations on these hosts in the Mediterranean. Note that several spellings of Ione thoracica / thoracicus were incorrectly given by Bourdon (1968) in his synonymy list and are corrected herein.

Boyko et al. (2013) erred when they stated that Ione spp. were unlikely to occur on gebiid hosts and also in their agreement with Bourdon (1968) in discounting the earlier report by Fraisse (1877; 1878a) of I. thoracica from Upogebia pusilla (Petanga, 1792) (not U. stellata (Montagu, 1808)) . In addition, data from An et al. (2009) strongly support the rare occurrence of Ione spp. on gebiid hosts.

We consider the material from Nigeria reported by Olaosebikan (1986) to be distinct from Ione thoracica . The form of the females’ uropods is very different from that seen in any specimens of I. thoracica (based on material examined in this study, as well as illustrations from other papers, e.g., Reverberi & Pitotti 1943; Bourdon 1968) and the coxal plates of the first two pereomeres are not elongated as in true I. thoracica . Additionally, the host, Callichirus balssi (Monod, 1933) , and locality occur well outside of the range of I. thoracica . Callianassa balssi Monod, 1933 is the type species of Balsscallichirus Sakai, 2011 , but is better left in Callichirus Stimpson, 1866 , pending revision of these and related genera (Poore, pers. commun.).

Figures

FIGURE 1. A–C, Ione thompsoni Richardson, 1904 (YPM IZ 089393) ex Gilvossius setimanus (DeKay, 1844)). A, dorsal overview of female; B, ventral overview of female with male in situ; C, ventral overview of male. D, photograph of live male Callianassa truncata Giard & Bonnier, 1890 (NHMW 20514) from Croatia bearing Ione thoracica (Montagu, 1808) (NHMW 25810) in left branchial chamber. Scale bars:A–C = 2 mm; D = 5 mm.D courtesyof Peter Dworschak.

FIGURE 2. Variation in pleopod morphology of Ione thoracica (Montagu, 1808). A, pleopod 1 of specimen identified by Bonnier (1900) as Ione vicina Bonnier, 1900 from Naples, Italy, note short endopod (arrow); B, pleopod 1 of specimen identified by Bonnier (1900) as I. thoracica from unspecified locality, but most likely Wimereux, France, note long endopod (arrow); C, pleopod 1 of specimen from Volosko, Croatia (NHMW 25807 ex Callianassa truncata Giard & Bonnier, 1890); D, pleopod 1 of specimen from Lido di Staranzano, Italy (NHMW 25231 ex Pestarella tyrrhena (Petagna, 1792)); E, pleopod 1 of specimenfrom Volosko, Croatia (NHMW 25810 ex C. truncata); F, pleopod 1 of specimen from Hammamet, Tunisia (NHMW 25809 ex C. truncata). A, B from Bourdon 1968; not to scale. Scale bars: C–F = 0.5 mm.