Figures 12–17
Oniscus umbricatus Fabricius, 1775: 296.
Oniscus imbricatus.— Fabricius, 1787: 241.— Stebbing, 1893: 354.
Cymothoa imbricata.— Fabricius, 1793: 503; 1798: 304.
Cymothoa trigonocephala.— Milne Edwards, 1835: pl. 14, figs. 1–5.
Cymothoé à tête triangulaire.— Milne Edwards, 1835: pl. 14, figs. 1–5.
Meinertia trigonocephala.— Trilles, 1973 b: 1245, pl. I ( 8–9).
Ceratothoa imbricatus.— Maxwell, 1982: 341.
Ceratothoa Huttoni Filhol, 1885: 446, pl. LV (fig. 7), pl. XLIX (fig. 2) [new synonymy].
Meinertia huttoni.— Hutton, 1904: 262.— Thomson, 1913: 245.
Codonophilus huttoni.— Nierstrasz, 1931: 132.
Meinertia gaudichaudii.— Szidat, 1966: 1, figs. 1–16.
Meinertia trillesi Avdeev, 1979 a: 48, pls. 1–2 [new synonymy].
Ceratothoa trillesi.—Beumer, Ashburn, Burbury, Jetté & Latham, 1983: 31.— Trilles, 1994: 129.— Hine, Jones & Diggles, 2000: 79.— Bruce, Lew Ton & Poore, 2002: 172.
Ceratothoa gaudichaudii. — Avdeev, 1992: 16, figs. 2 ( 1).
Ceratothoa trigonocephala.— Avdeev, 1992: 16, figs. 2 ( 2–3).
Ceratothoa cf. imbricata.— Heagney, Gillanders & Suthers, 2013: 10, fig. 1 (a, b).
Ceratothoa imbricata.— Hadfield, Bruce & Smit, 2014 a: 26, figs. 15, 16, 21 (E).
Not Codonophilus imbricatus.— Lanzing & O’Connor, 1975: 355, figs. 1 (a –b) [= Ceratothoa banksii].
Not Codonophilus imbricatus.— Monod, 1931: 23; 1933 a: 153; 1933 b: 195.— Pillai, 1954: 14 [= Ceratothoa trigonocephala].
Not Meinertia imbricata.— Trilles, 1973 b: 1248, pl. II ( 10–11) [= Ceratothoa banksii].
Not Codonophilus imbricatus.— Hale, 1926: 223; 1927: 315; 1929: 263; 1937: 19; 1940: 303 [= Ceratothoa banksii].
Not Ceratothoa imbricata.— Hadfield, Bruce & Smit, 2014 a: 26, figs. 17, 18 [= Ceratothoa banksii].
Excluded (identity not known)
Cymothoa approximans White, 1847: 110.— Miers, 1884: 300 [nomen nudum].
Codonophilus argus Haswell, 1881: 471, pl. XVI, fig. 1.— 1882: 283.— 1885: 1001.— Stebbing, 1893: 356.— Barnard, 1940: 404.— Trilles, 1972: 5, 7.
Ceratothoa imbricata.— Miers, 1884: 300.— Haswell, 1885: 1001, 1003.— Thomson & Chilton, 1886: 153.— Ellis, 1981: 123.— Avdeev, 1982 a: 65; 1982 b: 69.— Trilles 1994: 120; 2008: 23.— Kensley, 2001: 232.— Trilles, Ravichandran & Rameshkumar, 2011: 446.
Meinertia imbricata.— Stebbing, 1902: 58; 1908–1910: 424; 1910: 219.— Hutton, 1904: 262.— Nierstrasz, 1915: 88; 1918: 119.— Barnard, 1925: 121.— Avdeev, 1978 b: 282.
Meinertia imbricata.— Chilton, 1911: 546, 567.
Codonophilus imbricata.— Barnard, 1940: 404, 491.— Kensley, 1978: 79, figs. 32 (e –f).
Codonophilus imbricatus.— Nierstrasz, 1931: 131.— Hurley, 1961: 268, 284.— Hewitt & Hine, 1972: 79, 97, 99, 108.— Stephenson, 1976: 167.— Hooper, 1983: 42.
Ceratothoa imbricatus.— Collette, 1974: 19.—Beumer, Ashburn, Burbury, Jetté & Latham, 1983: 31.— Hine, Jones & Diggles, 2000: 79.
Types and type locality. The holotype of Ceratothoa imbricata is deposited at The Natural History Museum, London ( BMNH 1979.403.1; from New Zealand; host unknown), and has been illustrated in detail by Hadfield et al. ( 2014 a). The type material of Ceratothoa trillesi (Avdeev, 1979) was deposited at the Russian Federal Fisheries Research Institute ( TINRO AGK 75028; from Australia – New Zealand region, from Trachurus declivis), but a recent search (see acknowledgements) failed to locate the type material. The holotype of Ceratothoa huttoni Filhol, 1885 is deposited at the National Museum, Paris ( MNHM from New Zealand from an unknown host).
Material examined. Non-type material published or identified by Hale: 1 ♀ ovig. ( 29 mm), Cape Jervis, NSW, 16 March 1909 (AM E 4841). 1 ♀ ovig. ( 20 mm), 2 ♂ immature (10, 10 mm), Shoalhaven Bight, NSW, 1909–1914, coll. FIS Endeavour (AM E 6599). 8 ♀ ovig. (22, 22, 23, 23, 24, 25, 25, 26 mm), 1 ♂ mature ( 26 mm), Port Jackson, NSW, August 1928, coll. D. G. Stead ( SAM C 2919). 1 ♀ ovig. ( 29 mm), from buccal cavity of Trachurus novaezelandiae, no locality, coll. H. M. Hale (AM G 5822).
South Australian material: 1 ♂ mature ( 26 mm), 1 ♂ immature ( 11 mm), Port Lincoln, 24 April 1949, from buccal cavity of greenback horse mackerel Trachurus declivis (Jenyns, 1841) ( SAM C 3160).
New South Wales material: 2 ♀ ovig. (29, 35 mm), 5 ♂ immature (6, 6, 12, 15, 16 mm), off Iron Ladder Beach, near box Head, Broken Bay, depth 6 m, 32 °32.00’S; 151 °20.00’E, 19 November 2002, from buccal cavity of Trachurus novaezelandiae Richardson, 1843, coll. Ian Graham (AM P 64007). 1 ♀ pre-ovig. ( 26 mm), 1 ♂ immature ( 12 mm), off Iron Ladder Beach, near box Head, Broken Bay, depth 5 m, 20 July 2002, from buccal cavity of Trachurus novaezelandiae coll. Ian Graham (AM P 88160). 1 ♂ mature ( 22 mm), 1 ♂ immature ( 14 mm), off Iron Ladder Beach, near box Head, Broken Bay, 33 °32.00’S; 151 °20.00’E, 21 June 2002, from buccal cavity of Trachurus novaezelandiae, depth 5 m, coll. Ian Graham ( P 62804). 7 ♀ ovig. (16, 17, 17, 17, 17, 17, 18 mm), 3 ♂ mature (8, 12, 15, mm), Bantry Bay, 22 May 1904, from buccal cavity of Trachurus novaezelandiae coll. H. M. Hale (AM P 4891). 5 ♀ ovig. (22, 23, 24, 30, 30 mm), 2 ♂ mature (24, 27 mm), 7 ♂ immature (10, 11, 11, 12, 13, 13, 14 mm), bought from Pyrmount Fish Market, Sydney, 30 October 1986, from buccal cavity of Trachurus novaezelandiae (labelled Trachurus mccullochi) (MTQ W 30408).
Tasmanian material: 1 ♀ ovig. ( 22 mm), SS01/ 97 Stn. 8, depth 1.312 m, 76.8 km south-southeast of South East Cape, Main Pedra Hill, Tasman Sea, 44 °26.00’S; 147 °13.00’E, 24 January 1997, coll. CSIRO, on FRV “Southern Surveyor” (AM P 74791). 8 ♀ ovig. (15, 17, 18, 18, 19, 21, 22, 22 mm), 1 ♂ mature ( 24 mm), 2 ♂ immature (9, 15 mm), off St. Helens, East Coast, 40 ° 18.89 ’S; 148 ° 33.02 ’E, 5–9 December 2011, from buccal cavity of Trachurus declivis, coll. Megan Stride on Australian Maritime College Bluefin Vessel (MTQ W 34278).
Victorian material: 10 ♀ ovig. (24, 25, 25, 25, 26, 27, 27, 29, 29, 30 mm), 1 ♂ mature ( 22 mm), 4 ♂ immature (13, 13, 13, 17 mm), SS 05/ 94 / 26, depth 34 m, near Wilson’s Promontory, 38 ° 58.02 ’S; 146 ° 34.02 ’E, 24 August 1994, coll. P. B. Berents on F. R. V “Southern Surveyor” (AM P 43964).
Queensland material: 1 ♀ ovig. ( 20 mm), trawled, 6 miles northeastern Caloundra, 27 February 1970, coll. F.J. Wallace on F.V. Gemini (MTQ W 5744).
Chilean material: 7 ♀ ovig. (28, 29, 30, 31, 32, 34, 35 mm), 6 ♂ immature (8, 12, 15, 15, 13, 15 mm), Coquimbo fish market, Chile, South America, 24 July 2006, coll. N. L. Bruce (MTQ W 34276) from buccal cavity of Trachurus declivis.
No locality: 16 ♀ ovig. (18, 19, 20, 21, 21, 21, 21, 23, 23, 24, 24, 25, 25, 25, 25, 34 mm), 15 ♂ mature (18, 22, 22, 22, 22, 24, 25, 26, 26, 26, 27, 27, 28, 28, 29 mm), 5 ♂ immature (11, 13, 13, 13, 15 mm), no host and locality data (AM P 4900).
Ovigerous female. Length 34 mm, width 16 mm. Tasmania, from the buccal cavity of Trachurus declivis (MTQ W 34278).
Body rhomboid, 2.5 times as long as greatest width, dorsal surface smooth and polished in appearance, widest at pereonite 4 and pereonite 5, most narrow at pereonite 1, lateral margin slightly convex. Cephalon 0.6 times longer than wide, visible from dorsal view, subtriangular. Frontal margin apex obtuse. Eyes trapezoid, 0.2 times width of head. Pereonite 1 with slightly produced anterior margin; 5–7 subequal in length. Coxae 2–3 posteroventral margins rounded; coxae 4–7 posteroventral margins acute. Pleonites posterior margin concave; pleonite 1 similar width as pleonites 2–5, visible in dorsal view; posterolateral margins of pleonite 2 narrowly rounded; pleonite 5 with posterolateral margins overlapped by lateral margins of pleonite 4. Pleotelson 0.5 times as long as anterior width, dorsal surface trisinuate, lateral margins weakly concave, posterior margin without median point.
Antennula comprised of 7 articles; peduncle articles 1 and 2 distinct and articulated; article 2 1.0 times as long as article 1; article 3 0.8 times as long as combined lengths of articles 1 and 2, 0.8 times as long as wide; extending to posterior margin of eye. Antenna comprised of 9 articles; peduncle article 3 0.4 times as long as article 2, 0.9 times as long as wide; article 4 1.1 times as long as wide, 2.3 times as long as article 3; article 5 0.5 times as long as article 4, 1.0 times as long as wide. Terminal article without setae, extending past posterior margin of pereonite 1. Labrum lateral margins convex, anterior margin rounded. Maxillula simple, with 4 terminal robust setae. Maxilla mesial lobe partly fused to lateral lobe, covered in pectinate scales; 6 recurved robust setae on mesial lobe; 6 large recurved robust setae on lateral lobe. Maxilliped covered in pectinate scales, comprised of 3 articles, with lamellar oostegite lobe, article 3 with 2 recurved robust setae. Oostegites margin covered in numerous plumose setae.
Pereopod 1 basis 1.9 times as long as greatest width; ischium 0.6 times as long as basis; merus proximal margin with bulbous protrusion; carpus with rounded proximal margin; propodus 1.6 times as long as wide; dactylus slender, 0.9 as long as propodus, 2.1 times as long as basal width. Pereopod 2 propodus 1.5 as long as wide; dactylus 0.7 as long as propodus. Pereopods 3–5 similar to pereopod 2. Pereopod 6 basis 0.8 times as long as greatest width, ischium 0.8 times as long as basis, propodus 1.3 as long as wide. Pereopod 7 basis 0.9 times as long as greatest width; ischium 0.7 as long as basis, with slight proximal bulbous protrusion; merus 1 as long as ischium; carpus 0.3 as long as ischium, without bulbous protrusion, 0.4 times as long as wide; propodus 0.8 as long as ischium, 1.1 times as long as wide; dactylus slender, 1.5 times as long as propodus, 2.7 times as long as basal width.
Pleopods with slight depression on central dorsal surface of each pleopod rami, exopod larger than endopod. Pleopod 1 exopod 0.9 times as long as wide, lateral margin distally concave, distally broadly rounded, mesial margin weakly produced; endopod 1.1 times as long as wide, lateral margin straight, distally broadly rounded, mesial margin slightly convex, peduncle 5.5 times as wide as long, without retinaculae. Pleopods 2–5 similar to pleopod 1, 3– 5 endopods proximal borders do not extend below exopod to peduncle. Medial margin robust, increasing in size from pleopods 1–5.
Uropod same length as pleotelson, peduncle 0.9 times longer than rami, peduncle lateral margin without setae; rami extending to pleotelson apex, apices broadly rounded. Endopod 2.8 times as long as greatest width, lateral margin distally concave, mesial margin weakly convex. Exopod extending to end of endopod, 5.0 times as long as greatest width, apically rounded, lateral margin weakly convex, terminating without setae.
Males. Similar to females but much smaller; body subparallel, body 2.2 times as long as wide. Chomatophores lightly scattered on body. Pereopods 4–7 without broad and sharp carinae basis and bulbous protrusion on ischium, dactyli long and slender.
Colour. Pale yellow to brown, with posterior margins of pereonites dark brown to grey.
Variation. Eyes either trapezoid or round, prominent or vaguely visible; cephalon shape either subtriangular or with subacute rostrum, nearly immersed in anterolateral projections of pereonite 1 or visible cephalon with minute anterolateral projections of pereonite 1; body rhomboid or subparallel in shape; coloration of pereonites posterior region darkened or scattered darkened patches; pleotelson width occasionally appears raised; uropod extend beyond or lay hidden under pleotelson posterior margin, apically sharp or blunt; pereopods 4–7 with or without broad and sharp carinae basis and with or without bulbous protrusion on ischium.
Size. Present material: Ovigerous female: 35 – 15 mm (mean= 23.3 mm, N= 63), pre-ovigerous female: 26 mm, mature male: 8–29 mm (mean= 22.3 mm, N= 27), immature male: 6–16 mm (mean= 11.9 mm, N= 24).
Remarks. Ceratothoa imbricata can be identified by the rhomboid body shape with pereonites 1–4 progressively increasing in width, each pereonite with straight lateral margins; pereonites 5–7 progressively decreasing in width, each pereonite with convex lateral margins, convex anterolateral margins of pereonite 1, posterior margins of pereonites dark brown, and pleotelson narrower than pereonite 7.
Ceratothoa imbricata is most similar to C. banksii and C. trigonocephala, all three species with the antennula more stout than the antenna, pereonite 1 anterolateral margin pronounced or narrow, broad carina on pereopods 5– 7 basis and uropods extending to or slightly beyond the pleotelson margin. C. imbricata can be distinguished from C. trigonocephala by the rhomboid-shaped body (narrow subparallel body shape in C. trigonocephala); pleonite and pleotelson width similar or less than pereonite 7 and darker colouration on the posterior regions of the pereonites. The holotype of Ceratothoa banksii has body proportions 1.6 times as long as greatest width ( 2.1 times as long as greatest width in C. imbricata and 2.4 times as long as greatest width in C. trigonocephala), a rough dorsal surface and subtruncate pleotelson posterior margin. Ceratothoa trigonocephala has a distinctly subtriangular cephalon anterior margin, narrow and elongated body (pereonite 2–4 similar length), and subparallel body lateral margin. The differences mentioned for the above three species are those of ovigerous females and such body proportions very greatly according to the reproductive state of the female.
Ceratothoa imbricata is host specific to Trachurus declivis and Trachurus novaezelandiae (family Carangidae) whereas C. banksii occurs on several host taxa (see section on C. banksii). The preferred hosts and geographical distribution of C. trigonocephala remain unknown ( Hadfield et al. 2014 a).
Cymothoa approximans White, 1847 was recorded from Calcutta, without description, drawing, or hostassociation and is a nomen nudum. Miers ( 1884) regarded Cymothoa approximans as a junior synonym of Ceratothoa imbricata. It is here excluded from synonymy as there is no further information about this species.
Hurley ( 1961) in a footnote compared Filhol’s ( 1885) figures of Ceratothoa huttoni with Hale’s ( 1926) description of C. imbricata and considered that the species were the same. After reviewing Filhol’s ( 1885) drawings of C. huttoni, the distinctive rhomboid-shaped body and small pleotelson confirms this species as a junior synonym of C. imbricata.
Avdeev’s ( 1979 a) drawings of C. trillesi are similar to the holotype illustrations of Hadfield et al. ( 2014 a) and our present non-type material, showing characteristics of the pleotelson being narrower than pereonite 7, strong carina on pereopod 7 basis, body lateral margins subparallel from pereonites 1–3 and an increase from pereonites 4 and 5, relative decrease of width from pereonite 6 and 7. We requested a loan of the type material of C. trillesi, but the specimen could not be located. Avdeev’s ( 1979 a) description, illustrations, and the host association with Trachurus declivis nonetheless support a synonymy with C. imbricata.
Adult female specimens (MTQ W 34276) from Coquimbo from the host Trachurus murphyi are morphologically identical to the Australian specimens of Ceratothoa imbricata. Avdeev ( 1992) postulated that C. gaudichaudii and C. trigonocephala ( C. trigonocephala illustrations in Avdeev ( 1992) are here identified as C. imbricata) had transoceanic distributions, with both species using the host genus Trachurus. Trachurus murphyi is known to occur from South America to the Tasman Sea and off South Island, New Zealand ( Avdeev 1992). Figures for C. gaudichaudii given by Szidat ( 1966) and Avdeev ( 1992) are also in agreement with the holotype of C. imbricata and the Australian material examined herein and identified as C. imbricata. Ceratothoa gaudichaudii is here regarded as species inquirenda (p. 36). C. imbricata is known to occur on the host Trachurus murphyi from the eastern Pacific.
Codonophilus argus Haswell, 1881 was described from a manca from the bell of the jellyfish Rhizostoma Cuvier, 1800 from Port Jackson ( Haswell 1881) and from the jellyfish Catostylus mosaicus (Quoy & Gaimard, 1824; as Crambessa mosaica Haeckel, 1880). Codonophilus argus was later synonymised with Ceratothoa imbricata by Hale ( 1926). Identification of a manca to species level is nearly impossible without an associated adult female, and the association with a jellyfish as a host is likely to be accidental. We have here excluded Codonophilus argus from synonymy until further verification of the species is made (i.e. molecular identification).
Distribution. Present material from Australia: Port Lincoln, South Australia; Port Jackson, Cape Jervis, Broken Bay, Pyrmount and Caloundra, New South Wales; Wilson’s Promontory, Victoria; Tasman Sea and St. Helens, Tasmania. Previous reports include New Zealand ( Fabricius 1775; 1793).
Hosts. Present material was taken from Trachurus declivis and Trachurus novaezelandiae. Previous accounts have reported C. imbricata on Trachurus declivis ( Hale 1926, 1929; Stephenson 1976; Avdeev 1979 a; Maxwell 1982; Hooper 1983; Hine et al. 2000), Trachurus novaezelandiae ( Hewitt & Hine 1972; Stephenson 1976; Hine et al. 2000); Trachurus mccullochi ( Hooper 1983). Hale’s (1926, 1927, 1929) material of C. imbricata has been reidentified as C. banksii. Other accounts are from catalogues of cymothoids present in the Australian fauna, and as such we are unable to verify the specimen identity, therefore these accounts are excluded from the synonymy.
Stephenson ( 1976) reported the occurrence of C. imbricata on garfish Hyporhampus ihi but as we are unable to locate Stephenson’s ( 1976) specimen, the identity remains uncertain. Bruce & Bowman ( 1989) and Hadfield ( 2012) have not recorded C. imbricata from fish hosts in the family Belonidae.