Parapenaeon japonica (Thielemann, 1910)

(Figures 1–3)

Epipenaeon japonica Thielemann, 1910: 7, 79–81, 106–107, 108; text-figs. 86, 87; tab. 8; pl. II, fig. 31 (Okayama, Japan; infesting ‘ Penaeus sp.’). Chopra, 1923: 454, 458. Nierstrasz and Brender à Brandis, 1929: 302. Hiraiwa, 1933: 49–69; text-figs. 1–23; pl. I [Hiroshima Bay; infesting Metapenaeopsis barbata (de Haan), Metapenaeopsis acclivis (Rathbun) and Metapenaeopsis lamellata (de Haan)]. Monod, 1933: 222. Hiraiwa, 1934: 45–62, figs. 1–14 (Hiroshima Bay, Japan; infesting M. barbata). Hiraiwa, 1936: 101–137; pls. 1–7. Reverberi, 1942: 60. Reverberi and Pitotti, 1942: 116, 123. Nataraj, 1943: 58 (Travancore, India; infesting unidentified penaeoid). Morita, 1949: 211. Morris, 1948: 4. Qazi, 1959: 56, 59–60. Dale, 1979: 2, 4. Ivanov, 1982: 197. Wägele, 1989: 215. Cash and Bauer, 1993: 123.

Epipenaeon japonicum . Nierstrasz and Brender à Brandis, 1923: 68. Barnard, 1925: 408 (Delagoa Bay, Mozambique; infesting Penaeopsis monoceros Fabricius). Barnard, 1925b: 121 (same record). Barnard, 1940: 494. Monod, 1933: 220. Shiino, 1934: 260 (transferred to Apopenaeon). Veillet, 1945: 282. Morris, 1948: 14. Kensley, 1978: 152, 153, fig. 67H. Bourdon, 1979a: 480 (transferred to Parapenaeon). Sindermann, 1990: 196.

Apopenaeon japonicum . Shiino, 1934: 260–263, fig. 2 (Tanabe Bay, Japan; infesting M. barbata). Shiino, 1939: 80, fig. 1 (Tuyasaki, Fukuoka Prefecture, Kyûsyû, Japan; infesting M. acclivis). Reverberi, 1949: 45–47; figs. 37, 38. Shiino, 1950: 157. Bourdon, 1968: 133, 134, 386. Beck, 1979: 444. Beck, 1980: 148, 150, 152. Trilles, 1999: 332.

Epipenaeon japonicus . Hiraiwa and Sato, 1939: 105–115, 121–122 (Hiroshima, Japan; infesting M. barbata). Reverberi, 1943: 45, fig. 37. Reverberi, 1949: 45–47, figs. 37–38. Morris, 1948: 7, 14. Baffoni, 1950: 215. Sindermann and Rosenfield, 1967: 361. Sindermann, 1970: 171. Devi, 1987: 23, 26–27, 31, 32, tab. 1 {Kakinada, India; infesting Penaeus japonicus Bate [= Marsupenaeus japonicus (Bate)]}.

Apopenaeon japonicum var. hiraiwai Shiino, 1950: 151–155, fig. 1 (Kutino, Izo, Japan; infesting M. acclivis). Shiino, 1958: 51–53; fig. 13, tab. I; pl. III, fig. 7 {several localities in Japan; infesting M. acclivis; Momotori and Owase Bay, Japan; infesting Penaeopsis akayebi (Rathbun) [ Parapenaeus akayebi (Rathbun) = Metapenaeopsis bartata (de Haan)]}. Strömberg, 1971: 6, 7, 29, 31, 33, 34, 39, 42.

Epipenaeon qadrii Qazi, 1959: 57–60; figs. 1–6 [Korangi, Pakistan; infesting Parapenaeopsis stylifera (H. Milne Edwards)]. Bourdon, 1968: 331. Ahmed, 1978: 318–320 (Karachi, Pakistan; infesting P. stylifera). Bourdon, 1981: 242 footnote. Ahmed and Hakeem, 1982: 316–317; tab. I (coast of Pakistan; infesting P. stylifera). Owens, 1986: 14; tab. 2.4.1. Janssen and Brandt, 1994: 22. Kazmi and Tirmizi, 1994: 171, 173, 174; fig. 2 {Karachi, Pakistan; infesting Parapenaeopsis sculptilis (Heller) [= Mierspenaeopsis sculptilis (Heller)] and P. hardwickii (Miers) [= Mierspenaeopsis hardwickii (Miers)]}. Kazmi and Bourdon, 1997: 59 (considered synonym of Parapenaeon japonica). Kensley, 2001: 223. Fatima, 2001: 171–172. Hussain, 2001: 66.

Epipenaeon qadrrii [sic]. Qazi, 1959: 62 -A.

? ‘Bopyrid parasites’ [in part]. Cheung, 1963: 428 (Hong Kong; infesting many species of five penaeid genera).

Epipenaeon quadrii [sic]. Bourdon, 1968: 327. Ayub and Ahmed, 2004: 225. Owens, 1987: 118. Ayub, 1998: 219.

Apopenaeon japonicum hiraiwai . Strömberg, 1971: 6, 7, 29, 31, 33–34, 39, 42. Shiino, 1950: 155. Palisoc, 1987: 286.

Apopenaeon japonica . Shiino, 1950: 155.

Parapenaeon japonicum . Bourdon, 1979a: 480–486, figs. 6–7 [Madagascar; infesting Metapenaeus monoceros (Fabricius) and Penaeus semisulcatus de Haan]. Bourdon, 1979b: 432 {Gulf of Martaban, Burma; infesting Parapenaeopsis sculptilis (Heller) [= Mierspenaeopsis sculptilis (Heller)]}. Branford, 1980: 276, tab. 1 {Red Sea; infesting Penaeus latisulcatus Kishinouye [= Melicertus latisulcatus (Kishinouye)]}. Ivanov, 1982: 196 (Western Indian Ocean; infesting M. monoceros). Miquel, 1982: 94. Markham, 1986: 159. Anderson, 1990: 290. Courtney, 1991: 615, 617, 620; tab. 2 {Central coast of Queensland, Australia; infesting Penaeus longistylus Kubo [= Melicertus longistylus (Kubo)]}.

Parapenaeon japonica Markham, 1982: 366–369, 385, figs. 23–24 [Pearl River Estuary, Hong Kong; infesting Penaeus japonicus (= Marsupenaeus japonicus)]. Markham, 1985: 3, 50–51, 63; tab. {Chonburi, Thailand; infesting Trachypenaeus fulvus Dall [= Trachysalambria fulvus (Dall)]}. Owens, 1990: 35, 37; tab. 1. Owens, 1993: 381, 384, 386 [Northeast Australia; infesting P. longistylus (= M. longistylus) and P. latisulcatus (= M. latisulcatus); hyperparasitized by Cabirops orbionei Bourdon]. Markham. 1994: 240–242; figs. 10–11. [Strait of Makassar; infesting Metapenaeopsis sinica Liu and Zhong; Madagascar; infesting M. hilarula (de Man)]. Chu and Leong, 1996: 835. Kazmi and Bourdon, 1997: 59. An, 2006: 82–87; fig. 76 (South China Sea, Beibu Gulf, East China Sea; material examined in present report).

Epipenaeon . Wilson, 1991: 239, fig. 13.4.

Epipenaeum [sic] japonica . Janssen and Brandt, 1994: 9.

non Parapenaeon japonica . Kazmi and Tirmizi, 1994: 171, 172, 174; fig. 1 {Karachi, Pakistan; infesting Penaeus merguiensis de Man [= Fenneropenaeus merguiensis (de Man)]}. (= Parapenaeon expansa Bourdon, 1979a, below.)

‘[S]ome parasitic isopoda .’ Torres-García and Bortolini-Rosales, 2002: 63.

‘[B]opyrids.’ Ayub and Ahmed, 2004: 228.

Material examined

Infesting Metapenaeopsis toloensis Hall, 1962 . CIEPE730301, ♀, ♂, Beibu Gulf, Stn. 7303, 20°25 ′ N, 107°50 ′ E, 35 m, 25 August 1962, coll. Fuzeng Sun. CIEPE624901, ♀, ♂, Beibu Gulf, Stn. 6249, 20°15 ′ N, 107°30 ′ E, 35 m, 14 April 1960, coll. Fuzeng Sun. CIEPE621602, ♀, Beibu Gulf, Stn. 6216, 20°25 ′ N, 108°50 ′ E, 61.5 m, 15 April 1960, coll. Fuzeng Sun.

Infesting M. barbata (de Haan, 1844) . CIEPE413401, ♀, ♂, East China Sea, Stn. 4134, 29°30 ′ N, 123°00 ′ E, 59 m, 10 July 1959, coll. Liren Chen. CIEPE413402, ♀, ♂, East China Sea, Stn. 4134, 29°30 ′ N, 123°00 ′ E, 59 m, 10 July 1959, coll. Liren Chen. CIEPE408001, ♀, ♂, East China Sea, Stn. 4080, 28°00 ′ N, 122°00 ′ E, 52 m, 7 April 1959, coll. Yulin Liao. CIEPE413403, ♀, ♂, East China Sea, Stn. 4134, 29°30 ′ N, 123°00 ′ E, 59 m, 10 July 1959, coll. Liren Chen. CIEPE404602, ♀, ♂, East China Sea, Stn. 4046, 30°30 ′ N, 123°30 ′ E, 63 m, 10 August 1959, coll. Yuhang Cui. CIEPE404901, ♀, the East China Sea, Stn. 4049, 30°15 ′ N, 123°30 ′ E, 57 m, 23 October 1959, coll. Yuhang Cui. CIEPE413404, ♀, ♂, East China Sea, Stn. 4134, 29° 30 ′ N, 123°00 ′ E, 61 m, 17 April 1959 . CIEPE602601, ♀, ♂, South China Sea, Stn. 6026, 22°30 ′ N, 115°30 ′ E, 29 m, 16 July 1959, coll. Jingzuo, Qu. CIEPE615601, 2♀♀, 2♂♂, South China Sea, Stn. 6156, 18°45 ′ N, 110°45 ′ E, 118.5 m, 16 July 1959, coll. Ruiyu Liu. CIEPE404201, ♀, ♂, East China Sea, Stn. 4042, 31°00 ′ N, 123°30 ′ E, 55 m, 11 August 1959 . CIEPE405001, ♀, ♂, East China Sea, Stn. 4050, 30°00 ′ N, 123°30 ′ E, 61 m, 4 February 1959, coll. Liren Chen. CIEPE606201, ♀, ♂, South China Sea, Stn. 6062, 21°45 ′ N, 113°30 ′ E, 35 m, 24 April 1959, coll. Fuzeng Sun. CIEPE413405, ♀, ♂, East China Sea, Stn. 4134, 29°30 ′ N, 123°00 ′ E, 59 m, 10 July 1959, coll. Liren Chen. CIEPE406201, ♀, ♂, East China Sea, Stn. 4062, 29°00 ′ N, 122°30 ′ E, 46 m, 2 April 1959, coll. Yulin Liao. CIEPE605901, ♀, ♂, South China Sea, Stn. 6059, 21°30 ′ N, 113°45 ′ E, 44.5 m, 10 January 1959, coll. Baoling Wu. CIEPE404601, ♀, ♂, East China Sea, Stn. 4046, 30°30 ′ N, 123°30 ′ E, 57 m, 22 October 1959, coll. Liren Chen. CIEPE622201, ♀, Beibu Gulf, Stn. 6222, 18°45 ′ N, 108°30 ′ E, 23 m, 26 January 1959, coll. Zhengang Fan. CIEPE606401, ♀, ♂, South China Sea, Stn. 6064, 21°15 ′ N, 113°30 ′ E, 52 m, 18 October 1959, coll. Fengshan Xu. CIEPE405501, ♀, ♂, East China Sea, Stn. 4055, 29°30 ′ N, 124°00 ′ E, 74 m, 9 July 1959, coll. Liren Chen. CIEPE609101, ♀, ♂, South China Sea, Stn. 6091, 20°30 ′ N, 112°30 ′ E, 78 m, 5 July 1959, coll. Xiutong Ma. CIEPE607701, ♀, ♂, South China Sea, Stn. 6077, 21°00 ′ N, 113°00 ′ E, 64 m, 7 April 1959, coll. Zhican Tang. CIEPE606202, ♀, ♂, South China Sea, Stn. 6062, 21°45 ′ N, 113°30 ′ E, 32 m, 18 October 1959, coll. Yongliang Wang. CIEPE606501, ♀ (immature), South China Sea, Stn. 6065, 21°00 ′ N, 113°30 ′ E, 74 m, 14 July 1959, coll. Xiutong Ma. CIEPE602301, ♀, ♂, South China Sea, Stn. 6023, 21°45 ′ N, 116°00 ′ E, 103 m, 19 July 1959, coll. Weiquan Zhang. CIEPE751001, ♀, ♂, East China Sea, Stn. V-3, 27° 30 ′ N, 122°00 ′ E, 75 m, 11 October 1975, coll. Zhican Tang and Jieshan Xu.

Infesting Metapenaeopsis stridulans (Alcock, 1905) . CIEPE626201, ♀, ♂, Beibu Gulf, Stn. 6262, 19°30 ′ N, 107°00 ′ E, 49.6 m, 7 July 1960, coll. Zhengang Fan. CIEPE720401, ♀, Beibu Gulf, Stn. 7204, 20°30 ′ N, 108°30 ′ E, 49 m, 24 April 1962, coll. Fuzeng Sun. CIEPE625001, ♀, ♂, Beibu Gulf, Stn. 6250, 20°00 ′ N, 107°30 ′ E, 30.5 m, 11 July 1960, coll. Fuzeng Sun. CIEPE627001, ♀, ♂, Beibu Gulf, Stn. 6270, 19°30 ′ N, 108°30 ′ E, 35 m, 8 February 1960, coll. Fuzeng Sun. CIEPE760201, ♀, ♂, Beibu Gulf, Stn. 7602, 19°00 ′ N, 108°00 ′ E, 27 m, 11 April 1962, coll. Fuzeng Sun. CIEPE626301, ♀, Beibu Gulf, Stn. 6263, 19°00 ′ N, 107°00 ′ E, 55.5 m, 17 May 1960, coll. Zhengang Fan. CIEPE624301, ♀, ♂, Beibu Gulf, Stn. 6243, 18°00 ′ N, 108°00 ′ E, 90.8 m, 12 July 1960, coll. Shoupeng Shen. CIEPE619701, ♀, ♂, Beibu Gulf, Stn. 6197, 21°00 ′ N, 109°00 ′ E, 26 m, 17 July 1960, coll. Fuzeng Sun. CIEPE624001, ♀, ♂, Beibu Gulf, Stn. 6240, 19°30 ′ N, 108°00 ′ E, 58 m, 9 February 1960, coll. Zhengang Fan. CIEPE626601, ♀, Beibu Gulf, Stn. 6266, 17°30 ′ N, 107°00 ′ E, 52 m, 24 October 1960 . CIEPE625401, 2♀♀, ♂, Beibu Gulf, Stn. 6254, 18° 30 ′ N, 107°30 ′ E, 72 m, 25 May 1960 , coll., Fuzeng Sun.

Infesting Metapenaeopsis dura Kubo, 1949 . CIEPE730302, ♀, Beibu Gulf, Stn. 6203, 18°15 ′ N, 109°00 ′ E, 35 m, 25 August 1962, coll. Fuzeng Sun. CIEPE730501, ♀, Beibu Gulf, Stn. 7305, 20°00 ′ N, 108°30 ′ E, 20 April 1962 .

Infesting Metapenaeopsis mogiensis Rathbun, 1902 . CIEPE601113, ♀, ♂, South China Sea, Stn. 6011, 22°45 ′ N, 117°00 ′ E, 40.5 m, 5 January 1960 . CIEPE601114, ♀, ♂, South China Sea, Stn. 6011, 22°45 ′ N, 117°00 ′ E, 38 m, 24 April 1959, coll. Mu Chen. CIEPE601202, ♀, ♂, South China Sea, Stn. 6012, 22°30 ′ N, 117°00 ′ E, 47.6 m, 20 July 1959 .

Infesting Metapenaeopsis lamellata (de Haan, 1844) . CIEPE600501, ♀, ♂, South China Sea, Stn. 6005, 23°15 ′ N, 117°30 ′ E, 40 m, 24 April 1960, coll. Jingzuo, Qu.

Infesting Metapenaeopsis novaeguineae (Haswell, 1879) . CIEPE611901, ♀, ♂, South China Sea, Stn. 6119, 20°15 ′ N, 111°30 ′ E, 71 m, 26 January 1959, coll. Yongliang Wang. CIEPE610601, ♀, ♂, South China Sea, Stn. 6106, 20°30 ′ N, 112°00 ′ E, 65 m, 28 October 1959, coll. Yongliang Wang. CIEPE609102, ♀ (immature), ♂, South China Sea, Stn. 6091, 20°30 ′ N, 112°30 ′ E, 78 m, 5 July 1959, coll. Xiutong Ma. CIEPE602201, ♀, ♂, South China Sea, Stn. 6022, 22°00 ′ N, 116°00 ′ E, 87 m, 19 July 1959, coll. Jingzuo Qu. CIEPE605401, ♀, ♂, South China Sea, Stn. 6054, 21°00 ′ N, 114°00 ′ E, 80 m, 10 July 1959, coll. Weiquan Zhang. CIEPE604801, ♀, ♂, South China Sea, Stn. 6048, 21°00 ′ N, 114°30 ′ E, 84.6 m, 10 July 1959, coll. Jingzuo Qu. CIEPE623801, ♀, ♂, South China Sea, Stn. 6238, 20°00 ′ N, 108°00 ′ E, 58 m, 18 April 1959, coll. Zhican Tang. CIEPE611902, ♀, ♂, South China Sea, Stn. 6119, 20°15 ′ N, 111°30 ′ E, 66 m, 16 July 1959, coll. Zhican Tang. CIEPE606502, 3♀♀, 3♂♂, South China Sea, Stn. 6065, 21°00 ′ N, 113°30 ′ E, 74 m, 14 July 1959, coll. Xiutong Ma. CIEPE612001, ♀, ♂, South China Sea, Stn. 6120, 20°00 ′ N, 111°30 ′ E, 81 m, 16 July 1959, coll. Zhican Tang. CIEPE606601, ♀, ♂, the South China Sea, Stn. 6066, 20° 30 ′ N, 113°30 ′ E, 89 m, 25 April 1959, coll. Fuzeng Sun.

Infesting unidentified Metapenaeopsis species. CIEPE103701, ♀, ♂, Zhejiang Province, Stn. 1037, 20°15 ′ N, 111°30 ′ E, 71 m, 12 August 1960, coll. Guangyu Lin and Baolin Zhang. CIEPE570701, ♀, ♂, Xinying, Hainan Province, 19°53 ′ N, 109° 30 ′ E, 30 July 1957 . CIEPE551201, ♀, ♂, Xincun, Hainan Province, 18°35 ′ N, 110° 10 ′ E, 21 December 1955 . CIEPE560401, ♀, Guangdong Province, 22°42 ′ N, 114° 30 ′ E, 27 April 1956 . CIEPE720501, ♀, ♂, Beibu Gulf, Stn. 7205, 20°16 ′ N, 109° 00 ′ E, 37 m, 21 January 1962, coll. Fuzeng Sun. CIEPE720502, ♀, ♂, Beibu Gulf, Stn. 7205, 20°16 ′ N, 109°00 ′ E, 35 m, 24 April 1962, coll. Fuzeng Sun. CIEPE750301, ♀, Beibu Gulf, Stn. 7503, 19°30 ′ N, 107°00 ′ E, 52 m, 22 August 1962 . CIEPE740301, ♀, ♂, Beibu Gulf, Stn. 7403, 19°50 ′ N, 107°00 ′ E, 38 m, 21 August 1962, coll. Fuzeng Sun. CIEPE550401, ♀, ♂, Hainan Province, Sanya, 18°15 ′ N, 109°30 ′ E, 14 April 1955 . CIEPE570702, 2♀♀, 2♂♂, Hainan Province, Xinying, 19°53 ′ N, 109°30 ′ E, 30 July 1957 .

Remarks

Parapenaeon japonica is a very widespread species, and was reported from the Red Sea through the Indian Ocean past Pakistan and India to Japan, the Philippines and China, including Hong Kong. This species has been thoroughly described and illustrated, and some aspects of its biology have been studied (Hiraiwa 1933, 1934, 1936). Shiino (1950) transferred it to the genus Apopenaeon as A. japonicum because its female has six pleomeres. Bourdon (1979a) later transferred this species to Parapenaeon as P. japonicum . In recording it from Indonesia, the Philippines and near Madagascar, Markham (1994) diagnosed its characters; the most distinctive feature of the female is that its short side bears coxal plates on only the first two pereomeres. Kazmi and Tirmizi (1994) reported P. japonica from Pakistan but illustrated the female with coxal plates on both sides of all pereomeres; therefore they actually had Parapenaeon expansa (discussed below) instead.

The present specimens display a moderate amount of morphological variation. Although a female (Figure 1) infesting M. toloensis Hall conforms well to the description of those from Hong Kong (Markham 1982), its accompanying male (Figure 1M, N) is more similar to that from Madagascar (Bourdon 1979a: fig. 6m). Among parasites (Figure 2) of M. stridulans, the posterior margin of the first oostegite (Figure 2F, G) of one female is unusual, and its male (Figure 2H) has black eyes. A female (Figure 3A–H) infesting M. barbata (de Haan) has many small differences, internal ridge of oostegite 1 simple and palp stout and straight. At the same time, the pleon of its male has a large midventral tubercule (Figure 3J). In another male (Figure 3N), the pleon is separated into three pleomeres rather than being unsegmented.

The host species M. toloensis, M. dura, M. mogiensis and M. novaeguineae have never before been reported to bear bopyrid parasites, whereas M. stridulans have been reported to bear Epipenaeon ingens Nobili, 1906 and Orbione thielemanni Nierstrasz and Brender à Brandis, 1931. With the addition of the new host records, P. japonica is now known to infest 21 different penaeoid host species, the most for any orbionine bopyrid species. It is also the most widespread geographically of any orbionine species.