Parasitic copepods of the family Lernanthropidae Kabata, 1979 (Copepoda: Siphonostomatoida) from Australian fishes, with descriptions of seven new species Author Boxshall, Geoff A. Author Bernot, James P. Author Barton, Diane P. Author Diggles, Ben K. Author Q-Y, Russell Author Atkinson-Coyle, Toby Author Hutson, Kate S. text Zootaxa 2020 2020-02-17 4736 1 1 103 journal article 24025 10.11646/zootaxa.4736.1.1 c76ec731-0dc9-4fc4-8ea4-d90d90da9438 1175-5326 3669745 970D7D36-6D8C-4463-B9EA-D3B8E191BE72 Lernanthropus alepicolus sp. nov. ( Fig. 8–9 ) Type material: Holotype ♀ and 14 paratype ♀♀ from Alepes apercna Grant, 1987 ( TC17073 ), Moreton Bay , Queensland , 13 January 2016 ; collected by G.A. Boxshall , QM Reg. Nos.W29478 ( Holotype ♀ ), W29479 ( paratype ♀♀ ). 8 paratype ♀♀ from A. apercna ( TC17052 ), Moreton Bay , Queensland , 12 January 2016 ; collected by G.A. Boxshall , NHMUK Reg. No. 2018.206–213. Etymology: the name of the new species combines the generic name of the host with –icola , meaning inhabitant. Description. Female body comprising cephalothorax and trunk ( Fig. 8 A–C): body length excluding fourth legs ranging from 3.67 to 3.94 mm , with mean of 3.79 mm (based on 10 specimens ). Cephalothorax comprising about 30% of total body length, about 1.1 times longer than wide; lateral margins convex, slightly expanded anterolaterally into ventrally-directed folds on either side of cephalothorax ( Fig. 8B ). Anterior part of trunk (second and third pedigerous somites) well delimited from posterior part by transverse groove; narrowest anteriorly, with prominent anterolateral lobes (shoulders), and widest posteriorly with rounded posterolateral lobes. Posterior part of trunk ( Fig. 8A ) bearing broad, rounded dorsal trunk plate covering entire abdomen including caudal rami, but with distal half of fourth legs visible in dorsal view; dorsal trunk plate with rounded posterior margin with minor irregularities and slight median indentation. Urosome ( Fig. 9A ) comprising fifth pedigerous somite fused to broad genital complex, indistinctly separated from unsegmented abdomen. Genital complex wider than long with conspicuous paired genital openings dorsolaterally and paired copulatory pores on ventral surface at extreme posterolateral corners (arrowed in Fig 9A ). Dorsal surface of genital complex ornamented with row of 4 sensillae dorsally. Abdomen about 1.2 times longer than wide, with median anal slit. Paired caudal rami located on ventral surface: each ramus about 2.7 times longer than wide; armed with 2 plumose setae dorsally near base, 1 short lateral seta and 2 short apical setae ( Fig. 9A ). Antennule ( Fig. 9B ) 6-segmented, segments 3 and 4 incompletely separated; some segments with irregular cuticular thickening; setal formula: 1, 3, 2, 1, 1, 11 + 2 ae. Parabasal flagellum lacking. Antenna ( Fig. 9C ) robust, comprising swollen corpus, bearing papilliform process on medial surface, and distal subchela armed with small process in zone of arthrodial membrane in articulation between corpus and subchela; distal claw with flattened area of less sclerotized cuticle on concave margin. Mandible slender, stylet-like, armed with 8 marginal teeth distally ( Fig. 9D ). Maxillule ( Fig. 9E ) bilobate, smaller lobe tipped with 1 spiniform element; larger lobe tipped with 3 unequal spiniform elements. Maxilla ( Fig. 9F ) 2-segmented: comprising proximal syncoxa (lacertus) and distal basis (brachium); basis ornamented with slender process distally; terminal claw armed with rows of sharp denticles along both edges. Maxilliped ( Fig. 9G ) 2-segmented; comprising massive corpus with papilliform process and rounded knob on myxal surface, and distal subchela; subchela comprising compound endopodal segment, bearing minute seta (arrowhead on Fig. 9G ) on concave margin and small knob-like process distally; terminal claw strongly curved. Leg 1 with protopodal part fused to somite; members of leg pair joined by slender intercoxal sclerite ( Fig. 9H ). Each leg biramous with outer plumose seta and short, stout inner spine on incorporated protopod; exopod 1-segmented, armed with 5 robust terminal spines with smooth margins; endopod 1-segmented, tapering distally, armed with terminal seta and ornamented with patches of spinules distally. Leg 2 ( Fig. 9I ) mounted on inflated subspherical prominence derived from incorporated protopod and armed with outer plumose seta: both rami 1-segmented; exopod distinct, armed with 4 small distal spines; endopod incompletely separated basally, armed with small seta. Leg 3 bilobate: both lobes lamellate; outer (exopodal) lobe shoehorn-like in shape and slightly longer than inner (endopodal) lobe: endopodal lamellae of leg pair together forming hollow, shoehorn-like lobe but lobes separate along inner margin, not fused ( Fig. 8C ); outer basal seta not observed. Leg 4 ( Fig. 9J ) biramous with both rami forming elongate flattened processes, proximal part broader but tapering in distal half to narrower distal part; outer basal seta present proximally on dorsal surface: lobes of similar length but inner (endopodal) lobe slightly longer than outer (exopodal). Leg 5 ( Fig. 9A ) represented by cylindrical lobe about 2.5 times longer than width at base; armed with outer basal seta located dorsally near mid-length, plus 1 minute knob on ventral surface and another on dorsal surface of distal part. FIGURE 7 . Lernanthropus abitocephalus Tripathi, 1962 , adult ♀. A, habitus, dorsal; B, urosome plus caudal rami, dorsal. Lernanthropus pomadasysis Rangnekar & Murti, 1961 , adult ♀. C, habitus, dorsal; D, urosome plus caudal rami, dorsal. Scale bars A, C, 0.5 mm; B,D, 200 μm. TABLE 2. Lernanthropus species reported from hosts of the family Carangidae
Lernanthropus species Host Locality Reference
L. alatus Pillai, 1964 Selaroides leptolepis (Cuvier, 1833) India (Kerala) Pillai, 1964
Alepes melanoptera (Swainson, 1839) Vietnam Kazachenko et al ., 2014
L. alepicolus sp. nov. Alepes apercna Grant, 1987 Queensland, Australia present account
L. corniger Yamaguti, 1954 * Megalaspis cordyla (Linnaeus, 1758) Indonesia; India; China; Taiwan; Japan; Malaysia; Thailand; Arabian Gulf Yamaguti, 1954 ; Pillai, 1985 ; Song & Chen, 1976 ; Liu et al ., 2009b ; Leong, 1986 ; Ho & Kim, 2004 ; Al - Niaeem et al ., 2013
Alepes djedaba (Forsskål, 1775) (as Carangoides malabaricus ) Arabian Gulf Al - Niaeem et al ., 2013
Alepes djedaba (Forsskål, 1775) (as Caranx djedaba ) South Africa Kensley & Grindley, 1973
Decapterus sp. off Hainan Island, China Song & Chen, 1976
L. giganteus Krøyer, 1863 Caranx hippos (Linnaeus, 1766) (as Caranx carangus ) Brazil; Senegal Krøyer, 1863 ; Delamare Deboutteville & Nuñes-Ruivo, 1954
Caranx crysos (Mitchill, 1815) Jamaica; off West Africa Wilson 1913 ; Capart, 1959
Caranx hippos (Linnaeus, 1766) Jamaica; Texas (USA); Senegal; Brazil Wilson, 1913 ; Pearse, 1952 ; Diebakate & Raibaut, 1996 ; Luque & Alves, 2001
Caranx ignobilis (Forsskål, 1775) Sri Lanka; Taiwan Kirtisinghe, 1964 ; Liu et al ., 2009b
Caranx latus Agassiz, 1831 Brazil Luque & Alves, 2001
Caranx melampygus Cuvier, 1833 Yemen; Sri Lanka Bassett-Smith, 1898a ; Kirtisinghe, 1964
Caranx hippos (Linnaeus, 1766) (as Caranx sansum ) Sri Lanka Kirtisinghe, 1964
Caranx senegallus Cuvier, 1833 Senegal Delamare Deboutteville & Nuñes-Ruivo, 1954
Caranx sexfasciatus Quoy & Gaimard, 1825 Taiwan Liu et al ., 2009b
......continued on the next page TABLE 1. (Continued)
Lernanthropus species Host Locality Reference
Carangoides ferdau (Forsskål, 1775) (as Caranx ferdau ) India Pillai, 1985
Hemicaranx bicolor (Günther, 1860) off West Africa Capart, 1959
Carangoides praeustus (Anonymous [Bennett], 1830) China Song & Chen, 1976
Selaroides leptolepis (Cuvier, 1833) (as Caranx leptolepis ) Kuwait Ho & Sey, 1996
L. gnathanodontus sp. nov . Gnathanodon speciosus (Forsskål, 1775) Queensland, Australia present account
L. indicus Pillai, 1967 Caranx hippos (Linnaeus, 1766) (as Caranx sansum ) India Pillai, 1967
Megalaspis cordyla (Linnaeus, 1758) Arabian Gulf Al-Ataby et al ., 2012
Alepes djedaba (Forsskål, 1775) (as Carangiodes malabaricus ) Arabian Gulf Al-Ataby et al ., 2012
L. koenigii Steenstrup & Lutken, 1861 ** Parastromateus niger (Bloch, 1795) India Pillai, 1985
L. micropterygis Richiardi, 1884 *** Seriola dumerili (Risso, 1810) (as Micropteryx dumerili ) Mediterranean Sea Richiardi, 1884 ; Brian, 1906
Seriola lalandi Valenciennes, 1833 (as Seriola aureovittata ) Red Sea Wilson, 1924
[as L. delamarei Marques, 1960 ] Seriola lalandi Valenciennes, 1833 São Tomé Marques, 1960
[as L. ecclesi Kensley & Grindley, 1973 ] Seriola lalandi Valenciennes, 1833 South Africa Kensley & Grindley, 1973
[as L. gisleri van Beneden, 1852 ] Lichia amia Linnaeus, 1758 Mediterranean Sea Brian, 1906
L. mitratus Shiino, 1959 Seriola sp. 06° 30’ N, 77° 53’W Shiino, 1959
L. robustus Pillai, 1964 Caranx sp. India Pillai, 1964
......continued on the next page TABLE 1. (Continued)
Lernanthropus species Host Locality Reference
L. seriolii Shishido, 1898 **** Seriola quinqueradiata Temminck & Schlegel, 1845 Japan Shishido, 1898
Seriola lalandi Valenciennes, 1833 Japan Izawa, 2014
Seriola hippos Günther, 1876 Queensland, Australia present account
[as L. paenulatus ] Seriola hippos Günther, 1876 South Australia, Australia Hutson et al . 2007b
[as L. paenulatus ] Seriola lalandi Valenciennes, 1833 Massachusetts, North Carolina (USA); Australia; New Zealand; Wilson, 1922 ; Rohde et al ., 1995 ; Hutson et al ., 2007a
[as L. paenulatus ] Seriola sp. China Song & Chen, 1976
Misidentified species
L. polynemi Richiardi, 1881 † [as L. trifoliatus Bassett-Smith, 1898 ] Alepes djedaba (Forsskål, 1775) (as Caranx kalla ) Sri Lanka Kirtisinghe, 1956
L. polynemi Richiardi, 1881 † [as L. trifoliatus Bassett-Smith, 1898 ] Carangoides praeustus (Anonymous [Bennett], 1830) (as Caranx Carangoides praeustus ) Sri Lanka Kirtisinghe, 1956
L. caranxi Hesse, 1878 †† “ Caranx brachurus ” European waters Hesse, 1878
* Lernanthropus corniger has also been reported from a number of non-carangid hosts including: Mene maculata (Bloch & Schneider, 1801) (Menidae) and Myripristis vittata Valenciennes, 1831 (Holocentridae) by Liu et al ., (2009b), and Rastrelliger brachysoma (Bleeker, 1851) (Scombridae) by Pillai (1985) . ** Lernanthropus koenigii has also been reported from the non-carangid host, Peprilus paru (Linnaeus, 1758) (Stromateidae) by Pillai (1985) ***Here we propose that L. ecclesi Kensley & Grindley, 1973 be recognised as a junior subjective synonym of L. micropterygis and that L. delamarei Marques, 1960 is tentatively considered to be a synonym of L. micropterygis . **** We consider that the report of L. seriolii (as L. paenulatus ) from Scienops ocellatus (Linnaeus, 1766) by Causey (1953) may be a misidentification. † Piasecki & Hayward (2002) concluded that Kirtisinghe’s material was unlikely to represent L. trifoliatus , which they synonymised with L. polynemi . †† Lernanthropus caranxi Hesse, 1878 is here transferred to Lernanthropinus as Lernanthropinus caranxi ( Hesse, 1878 ) n. comb . (see text). FIGURE 8 . Lernanthropus alepicolus sp. nov. , paratype ♀. A, habitus, dorsal; B, habitus, lateral; C, habitus, ventral. Scale bar 1 mm. Remarks: Globally, 13 species of Lernanthropus are typically found on carangid hosts ( Table 2 ). Six of these species are known only from host fishes belonging to the genus Seriola Cuvier, 1816 : L. delamarei Marques, 1960 , L. ecclesi Kensley & Grindley, 1973 , L. micropterygis Richiardi, 1884 , L. mitratus Shiino, 1959 , L. paenulatus Wilson, 1922 , and L. seriolii Shishido, 1898 . The adult females of L. micropterygis and L. ecclesi both have a long slen- der body form with a lanceolate leg 5 that is about 4 to 5 times longer than wide, and lanceolate caudal rami, the tips of which extend beyond the posterior margin of the dorsal trunk plate. Richiardi’s (1884) original description of L . micropterygis was based on females collected from Seriola dumerili (Risso, 1810) (as Micropteryx dumerili ). It was very brief and lacked illustrations, however Goggio (1906) subsequently illustrated the habitus of both sexes based on material from the same host also caught in Italian waters. Some further morphological details of L . micropterygis were provided by Wilson (1924) , based on material from Seriola lalandi Valenciennes, 1833 (as S. aureovittata ) caught in the Red Sea . The South African material from Seriola lalandi described by Kensley & Grindley (1973) as a new species, L. ecclesi , appears to be identical to L . micropterygis in all important respects. We here propose that L. ecclesi be treated as a junior subjective synonym of L . micropterygis . The female illustrated by Brian (1906 : Tav. XVII, fig. 2) under the name L. gisleri is misidentified: it is L . micropterygis and its host was the carangid Lichia amia Linnaeus, 1758 . Lernanthropus mitratus and L. seriolii both have long lanceolate fifth legs that extend well beyond the tips of the caudal rami. Both of these species and L . micropterygis can be readily differentiated from L. alepicolus sp. nov. by the fifth legs, which are reduced to a short, laterally-directed, cylindrical process in the new species, and which are only about the same length as the caudal rami. The fifth legs of L. paenulatus were described by Wilson (1922) as “a pair of short fifth leg rudiments just in front of the genital segment”, but re-examination of the type material of L. paenulatus has revealed that it has a large lanceolate leg 5. After more detailed consideration (see below) we conclude that L. paenulatus Wilson, 1922 is a junior subjective synonym of L. seriolii Shishido, 1898 . FIGURE 9 . Lernanthropus alepicolus sp. nov. , paratype ♀. A, urosome showing right leg 5 and caudal rami, dorsal; B, anten- nule; C, antenna; D, mandible; E, maxillule; F, maxilla; G, maxilliped; H, leg 1 and intercoxal sclerite; I, leg 2; J, leg 4. Scale bars A,C, 200 μm, B,F–I, 100 μm, E, 50 μm, J, 0.5 mm. Unfortunately, L. delamarei is known only from the male ( Marques, 1960 ) and the male of the new species is unknown. However, in Lernanthropus both sexes usually have very similar antennules: in L. delamarei the antennule is 7-segmented compared to indistinctly 6-segmented in the new species. It seems probable that L. delamarei is the male of one of the other species known from the Atlantic and Mediterranean, L. micropterygis and L. seriolii . Its body is less elongate than the male of L. micropterygis (as L. ecclesi ) figured by Kensley & Grindley (1973) , although this may well be a fixation artefact. The 7-segmented antennules and the presence of a single long seta on the apex of the endopod of legs 1 and 2 are shared characters. The body form of the male of L. seriolii is more similar to that of L. delamarei but the antennules are only 6-segmented and the endopod of leg 2 lacks an apical seta according to Wilson (1922 : Pl. 7, Fig. 56). We tentatively place L. delamarei into synonymy with L. micropterygis , but re-examination of these males is necessary to confirm its true identity. Among the remaining species listed in Table 2 , L. giganteus Krøyer, 1863 is the most widely distributed, occurring on at least 11 different species of four different carangid genera, Caranx Lacepède, 1801 , Carangoides Bleeker, 1851 , Hemicaranx Bleeker 1862 and Selaroides Bleeker, 1851 ( Table 2 ). It is characterized by the large processes on the posterolateral corners of the anterior part of the trunk, combined with the elongate fifth legs that extend at least to the tips of the elongate caudal rami (which are themselves about 4.2 times longer than wide, see Liu et al ., 2009b ). The new species differs in having short posterolateral processes on the anterior part of the trunk, short fifth legs that do not extend back past the genital apertures, and caudal rami that are only about 2.7 times longer than wide. The other widely distributed species, L. corniger Yamaguti, 1954 , is similar to the new species in having short fifth legs bearing a single subapical seta and it is also known to occur on a species of Alepes Swainson, 1839 ( Table 2 ). However, L. corniger is instantly recognizable by the conspicuous paired anterior processes on the dorsal cephalic shield, formed by anterior projections of the ventrally folded lateral margins of the shield. Such frontal processes are lacking in the new species. Lernanthropus robustus is another distinctive species, distinguishable by the shape of the dorsal trunk plate, which is longer than wide and has a concave posterior margin and angular posterolateral corners. In contrast the new species has a rounded dorsal trunk plate which is wider than long and has a rounded free posterior margin. Another major difference is leg 5, which is long and lanceolate in L. robustus but short with a single subapical seta in L. alepicolus sp. nov. The new species differs from L. indicus Pillai, 1967 in the form of leg 5, which is short with a single subapical seta in the former, but elongate in the latter, extending well beyond the tips of the caudal rami. The dorsal trunk plate of L. indicus is just longer than wide and tapers posteriorly whereas in the new species the plate is about 1.3 times wider than long and is widest at mid-length. Lernanthropus koenigii Steenstrup & Lutken, 1861 , which occurs on both a carangid and a stromateid host ( Pillai, 1985 ), is similar to L. indicus in habitus but has enormous fifth legs, which are only just shorter than the inner (endopodal) lobe of the fourth legs. This feature serves to distinguish L. koenigii from both L. indicus and the new species. The adult female of L. alatus Pillai, 1964 is similar in general habitus to L. alepicolus sp. nov. and both species have relatively short fifth legs that project laterally and do not extend past the genital openings. These species differ in the shape of the cephalothorax, which is about 1.3 times longer than wide with linear margins in the former but about as wide as long, with convex margins in the new species. In addition, the anterior trunk has pronounced anterior projections (“shoulders”) in L. alepicolus sp. nov. whereas in L. alatus these corners are rounded. Lernanthropus caranxi Hesse, 1878 is still listed in WoRMS as a valid species under the name L. carangis Hesse, 1878 (Walter & Boxshall, 2019) but, as already indicated by Wilson (1922) , it almost certainly doesn’t belong in Lernanthropus . Given the poor quality of the original description, the generic placement of this species appears problematic as it shows some similarities with both Lernanthropinus and Lernanthropodes , depending on the interpretation of Hesse’s description. Wilson (1922) simply rejected it from Lernanthropus but was “unable to locate it anywhere else”. Hesse’s (1878) description is stylized but shows the female with a deeply-incised dorsal trunk plate combined with paired third legs, as typical for a member of the genus Lernanthropinus . Its type host was given as “ Caranx brachurus ” by Hesse (1878) , but the name of the host cannot be traced: brachurus has never been used as a specific epithet for any member of the family Carangidae ( Eschmeyer, 1998 ) . We believe that brachurus is a typographical error for trachurus , because Caranx trachurus Linnaeus, 1758 (now known as Trachurus trachurus (Linnaeus, 1758)) is a common carangid in European waters. This is also the type host for Lernanthropinus trachuri (Brian, 1903) . Comparison between the figures of Lernanthropus caranxi published by Hesse (1878) and the descriptions of Lernanthropinus trachuri published by Brian (1903, 1906) shows no major differences that cannot be attributed to the descriptive standards of the late nineteenth Century. We, therefore, recognise L. trachuri as a junior subjective synonym of L. caranxi , and this species is transferred to Lernanthropinus as Lernanthropinus caranxi ( Hesse, 1878 ) n. comb. Its original spelling is retained and the amended spelling, L. carangis , used by Bassett-Smith (1899) , Goggio (1906) and Wilson (1922) can be considered an unnecessary emendation. Among species that do not occur on carangid hosts, the new species most closely resembles L. opisthopteri Pillai, 1964 , a parasite of Opisthopterus tardoore (Cuvier, 1829) in Indian coastal waters, a member of the family Pristigasteridae . The basic body shape is similar and both species have a short leg 5 armed with a single seta. However, in L. opisthopteri the lobes of leg 4 differ in length, with a longer outer (exopodal) lobe that is longer than the entire body, whereas in the new species the outer and inner lobes are subequal and both are shorter than the entire body. These comparisons with congeners from carangid hosts and with other congeners with similar body form, reveal multiple differences that justify the establishment of the new species to accommodate the Australian material collected from Alepes apercna .