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Redescription and molecular characterisation of the fish parasitic isopod Norileca indica (Milne Edwards, 1840) (Crustacea: Isopoda: Cymothoidae) with a key to the genus Redescription and molecular characterisation of the fish parasitic isopod Norileca indica (Milne...
van der Wal, Serita; Smit, Nico J; Hadfield, Kerry A
2017-07-03 00:00:00
African Zoology 2017, 52(3): 163–175 Printed in South Africa Copyright © The Authors Open Access article distributed under the terms of the AFRICAN ZOOLOGY Creative Commons Attribution License [CC BY 4.0] ISSN 1562-7020 EISSN 2224-073X (http://creativecommons.org/licenses/by/4.0) http://dx.doi.org/10.1080/15627020.2017.1382389 Redescription and molecular characterisation of the fish parasitic isopod Norileca indica (Milne Edwards, 1840) (Crustacea: Isopoda: Cymothoidae) with a key to the genus 1 1 1,2 Serita van der Wal , Nico J Smit and Kerry A Hadfield * Water Research Group, Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Potchefstroom, South Africa Department of Zoology and Entomology, University of the Free State, Bloemfontein, South Africa * Corresponding author, email: kerryh26@yahoo.com Norileca indica (Milne Edwards, 1840) is fully redescribed based on ovigerous females collected from Maputo Bay, Mozambique, from the branchial cavity of the fish host Selar crumenophthalmus Bloch, 1793. An identification key to the species of Norileca Bruce, 1990 is given. Furthermore, a fragment of the mitochondrial cytochrome oxidase I (COI) gene from N. indica was sequenced for the first time. This is the first molecular characterisation of a species of Norileca. Keywords: branchial cavity, cymothoid, genetic characterisation, Norileca, Selar crumenophthalmus, taxonomy Introduction Species of Norileca Bruce, 1990 inhabit the branchial Methods cavity of fish hosts and are commonly recorded from pelagic fishes (Rameshkumar et al. 2015). There are Norileca indica specimens were collected during November three known species: Norileca borealis Javed & Yasmeen, 2013 from the bigeye scad, Selar crumenophthalmus 1999, N. triangulata Richardson, 1910 and N. indica (Milne Bloch 1793 by local subsistence fishermen in Maputo Edwards, 1840). Norileca borealis was originally described Bay, Mozambique. Isopods were analysed following the from the northern Arabian sea (Javed and Yasmeen 1999), techniques of Hadfield et al. (2010, 2013). Species descrip- parasitising the Indian mackerel, Rastrelliger kanagurta tions were made with the aid of the taxonomy software Cuvier, 1817. No other recordings of this species have been package DELTA (Descriptive Language for Taxonomy) reported since its original description. Norileca triangulata (see Coleman et al. 2010), following a general Cymothoidae was first recorded from Tanimdao Island, the Philippines, character data set originally developed by Hadfield et al. without mention of a fish host (Richardson 1910). (2013) and recently updated (Hadfield et al. 2016). Ratios Specimens of N. triangulata have since been recorded and measurements for the description were made using from Australia (from Cape York, Great Barrier Reef and the maximum values at the middle of the specific measured south-eastern Queensland), from the branchial cavity of the article, and all proportional measurements were rounded sailfin flyingfish, Parexocoetus brachypterus Richardson, to one decimal place. Isopod classification follows Brandt 1846 and Sardinella gibbosa Bleeker, 1849 (Bruce and Poore (2003) and host nomenclature follows that of 1990). More recent recordings are from the Parangipettai FishBase (Froese and Pauly 2017) and Catalog of Fishes coastal waters on the south-east coast of India, from the (Eschmeyer et al. 2017). goldstripe sardinella, Sardinella gibbosa Bleeker, 1849 Genomic DNA was extracted from isopod pereopods and pleopods following the protocol for animal tissue extrac- (Rameshkumar and Ravichandran 2015). Norileca indica tion of the GeneJET™ Genomic Extraction Kit (Thermo was originally described by Milne Edwards (1840) as Scientific, Waltham, MA, USA). A targeted part of the Livoneca indica. It was later redescribed by Bruce (1990) mitochondrial cytochrome oxidase I (COI) gene (approxi- and transferred to the genus Norileca. mately 680 bp) of these specimens was subjected to PCR As part of a larger project on the global diversity of amplification with the aid of a Bio-Rad C1000 Touch™ cymothoids, N. indica specimens were collected from Thermal Cycler and universal invertebrate primers Maputo Bay, Mozambique, and provided the opportunity to LCO1490 (5′-GGTCAACAAATCATAAAGATATTGG-3′) and complete a redescription of this species based on ovigerous HC02198 (5′-TAAACTTCAGGGTGACCAAAAAATCA-3′) females. In addition, this paper also presents a detailed (Folmer et al. 1994). The PCR protocol followed that of redescription of the male, as well as the first molecular Ketmaier et al. (2008). PCR products were sequenced characterisation of this species and genus, using the in both directions by Inqaba Biotechnical Industries mitochondrial cytochrome oxidase I (COI) gene. African Zoology is co-published by NISC (Pty) Ltd and Informa UK Limited (trading as Taylor & Francis Group) 164 van der Wal, Smit and Hadfield (Pty) Ltd, Pretoria, South Africa. The bioinformatics peduncles (Bruce 1990). It can be distinguished from software platform, Geneious R9.1 (Biomatters, Auckland, other cymothoid genera by pleonite 1 being the widest of New Zealand; available at http://www.geneious.com), the pleonites, as well as its weakly twisted body shape was used to trim and align consensus sequences. (Hadfield 2012). Sequences were deposited into the NCBI GenBank database (http://www.ncbi.nlm.nih.gov/genbank/) with Key to the species of Norileca the following accession numbers: MF628258, MF628259 and MF628260. 1. Pleonite 5 narrower than pleonite 1; uropods almost reaching posterior margin of pleotelson; pleotelson Abbreviations approximately 0.9 times as long as wide .......................2 Pleonite 5 and pleonite 1 subequal; uropods two-thirds MNHN = National Museum of Natural History, Paris, the length of pleotelson; pleotelson approximately France; NWU = North-West University, Potchefstroom 1.0–1.2 times as long as wide ..........................N. indica Campus; SAM = Iziko South African Museum, Cape Town; 2. Body twisted to the side; maxilla medial lobe with TL = total length; W = width. 1 robust seta and lateral lobe with 4 robust setae ........... ...................................................................... N. borealis Taxonomy Body nearly straight; maxilla medial lobe with 2 robust setae and lateral lobe with 2 robust setae ....................... Suborder: Cymothoida Wägele, 1989 ..................................................................N. triangulata Superfamily: Cymothooidea Leach, 1814 Family: Cymothoidae Leach, 1814 Norileca indica Milne Edwards, 1840 Livoneca indica Milne Edwards, 1840: 262.—Bleeker, 1857: Genus Norileca Bruce, 1990 21, 28.—Gerstaecker, 1882: 261.—Schioedte & Meinert, Norileca Bruce, 1990: 289.—Bruce, Lew Ton & Poore 1884: 362–365, pl. 5, figs. 3–6; Richardson, 1910: 24.— 2002: 181. Nierstrasz, 1915: 99–100.—Nierstrasz, 1931: 142–143, 145.—Borcea, 1933: 482.—Beumer, Ashburner, Type species: Livoneca indica Milne Edwards, 1840, by Burbury, Jette & Latham, 1982: 33. original designation (Bruce 1990). Livoneca ornata Heller, 1868: 145–146, pl. 12, fig. 15.— Gerstaecker, 1882: 261. Diagnosis Lironeca indica.—Trilles, 1976: 777–778, pl. 2, fig. 3.— Body weakly vaulted dorsally, twisted to one side. Avdeev, 1978: 281–282.—Trilles, 1979: 266.—Rokicki, Cephalon posterior margin medially indented, weakly or not 1982: 205–208, figs. 1–2.—Trilles, 1994: 178–179. trilobed. Coxae narrow, shorter than, or as long as respec- Norileca indica.—Bruce, 1990: 291–293.—Bruce, Lew tive pereonites. Brood pouch with 4 pairs of alternately Ton & Poore, 2002: 181.—Ghani, 2003: 219.—Yu & overlapping oostegites on coxae 2–5. Pleon not immersed Li, 2003: 235–237, fig. 10.—Yamauchi, Ohtsuka & in pereon; pleonite 1 widest; pleonites 1–5 becoming Nagasawa, 2005: 25–27.—Nagasawa & Petchsupa, progressively narrower; pleonites 1 and 2 without ventro- 2009: 131–133.—Rameshkumar, Ravichandran & lateral processes. Uropods not extending beyond posterior Sivasubramanian, 2013a: 99–105.—Rameshkumar, margin of pleotelson. Pleopods 1–4 with laminar rami; Ravichandran, Sivasubramanian & Trilles, 2013b: peduncle articles 2–5 lateral margin with laminar lobe; 42–46.—Argente, Narido, Palla & Celedonio, 2014: endopods 3–5 folded proximomedial lobe present; endopod 3–8.—Neeraja, Tripathi & Shameem, 2014: 49–56.— 5 distal margin medially indented, including 2 folded lobes. Rameshkumar & Ravichandran, 2015: 33–36.— Pereopods lacking expanded lobes; without expanded Rameshkumar, Ramesh, Ravichandran, Trilles & carina on bases. Antennula shorter than, or subequal to Subbiah, 2015: 712–715.—Aneesh, Kappalli, Kottarathil, antenna; bases of antennula wide apart. Mandible palp Gopinathan & Trilles, 2015: 42.—Behera, Ghosh & article 2 flattened, prominently expanded. Maxilliped lacking Pattnaik, 2016: 856–862.—Jithin, Swapna, Kumar, oostegital lobes. Venu, Helna & Sudha, 2016: 47–53.—Cruz-Lacierda & Nagasawa, 2017: 60–63. Remarks Norileca shares several characters with Livoneca Type material: Holotype held at the Museum Nationale Leach, 1818. Both genera are similar with regard to their d’Histore Naturelle, Paris (MNHN-IU-2007-4159). pereopod morphology, all of which are robust and lacking Type locality: Sumatra Island, Indonesia (Milne Edwards an expanded carina on the base of the pereopods; the 1840). cephalon posterior margin is trilobed; and the pleon is Type host: No type host recorded. not immersed in the pereon with pleonites 1–5 becoming progressively narrower. Norileca can be distinguished from Material examined Livoneca in having a weakly trilobed cephalon (vs strongly Three ovigerous ♀ (33.0 mm TL, 16 mm W; 30.0 mm TL, 17 trilobed in Livoneca) and pleonites 1–3 lateral margins mm W; 26.0 mm TL, 13 mm W) and 1 ♂ (11.0 mm TL; 3.0 which are not bilobed. Norileca also has an expanded mm W), Maputo Bay, Mozambique, South Africa, November mandible palp article 3, pleopods 3–4 without folds on 2013, from bigeye scad Selar crumenophthalmus (Bloch, endopods, as well as an absence of branchiated pleopod 1793), coll. Wynand Vlok (SAMC-A089028). African Zoology 2017, 52(3): 163–175 165 Two ovigerous ♀ (29.0–35.0 mm TL; 15.0–19.0 mm W) Body twisted to the right side, 2.2 times as long as and 2 non-ovigerous ♀ (28.0–30.0 mm TL; 14.0–18.0 mm greatest width, dorsal surfaces smooth and polished W), Maputo Bay, Mozambique, South Africa, November in appearance, widest at pereonite 4, most narrow 2013, from bigeye scad Selar crumenophthalmus (Bloch, at pereonite 1. Pereonite lateral margins posteriorly 1793), coll. Wynand Vlok (in the collection of the authors at protruding. Cephalon 1.1 times longer than wide, visible NWU). from dorsal view, triangular. Frontal margin thickened and ventrally folded. Eyes oval with distinct margins, Ovigerous female one eye 0.3 times the width of the cephalon, 0.3 times (Figures 1–4) the length of the cephalon. Pereonite 1 smooth, with anterior border indented and anterolateral angle weakly Length 33.0 mm, width 16.0 mm. produced, extending to middle of cephalon. Coxae 2–3 Figure 1: Norileca indica (Milne Edwards, 1840) ovigerous female (33.0 mm TL, 16.0 mm W) (SAMC-A089028). (a) Dorsal body, (b) lateral body, (c) dorsal view of pleotelson with uropods, (d) dorsal view of cephalon and pereonite 1 166 van der Wal, Smit and Hadfield wide with posteroventral angles rounded; coxae 4–7 acute, Antennula consists of 8 articles; peduncle articles posteriorly pointed, not extending past pereonite margin. 1 and 2 distinct and articulated; article 2 1.1 times as Pereonites 6 and 7 narrower than pereonites 1–5. Pleon long as article 1; article 3 1.6 times as long as wide, with pleonite 1 slightly wider than other pleonites, visible 0.5 times as long as combined lengths of articles 1 and in dorsal view; pleonites posterior margin not smooth, 2; flagellum with 5 articles, extending to posterior margin medially produced. Pleonite 2 partially overlapped by of eye with tufts of simple setae on articles 3–6 and 8. pereonite 7 posterolateral margin; posterolateral angles Antenna consists of 9 articles; peduncle article 3 1.0 times of pleonite 2 rounded. Pleonites 3–5 similar in form to as long as article 2; article 4 2.2 times as long as wide, pleonite 2; pleonite 5 free, not overlapped by lateral 1.4 times as long as article 3; article 5 twice as long as margins of pleonite 4. Pleotelson as long as anterior wide, 0.7 times as long as article 4. Antenna flagellum width; dorsal surface smooth; lateral margins weakly with 6 articles, terminal article with 1–5 short simple setae, convex, posteriorly narrow; posterior margin converging to extending to anterior margin of pereonite 1. Mandibular caudomedial point. molar process present, with no simple setae; mandible Figure 2: Norileca indica (Milne Edwards, 1840) ovigerous female (33.0 mm TL, 16.0 mm W) (SAMC-A089028). (a) Antennula, (b) antenna, (c) mandible, (d) maxilliped, (e) tip of maxillule, (f) tip of maxilliped article 3, (g) maxilla African Zoology 2017, 52(3): 163–175 167 palp article 2 and 3 without setae. Maxillule simple with merus proximal margin with large bulbous protrusion; 4 terminal robust setae. Maxilla medial lobe partly fused 0.4 times as long as wide, 0.3 as long as ischium; carpus to lateral lobe; medial lobe with 2 recurved robust setae, 0.4 times as long as wide, 0.2 as long as ischium, with lateral lobe with 1 large recurved robust setae. Maxilliped slight bulbous protrusion; propodus as long as wide, 0.4 as palp article 2 without setae; article 3 with 4 recurved long as ischium; dactylus slender, 1.9 as long as propodus, robust setae. 2.7 times as long as basal width. Pereopod 1 basis 1.8 times as long as greatest width; Pleopods without setae, exopod larger than endopod. ischium 0.7 times as long as basis; merus proximal margin Pleopod 1 exopod 1.1 times as long as wide, lateral margin with bulbous protrusion; carpus with straight proximal weakly convex, distally broadly rounded, medial margin margin; propodus 1.1 times as long as wide; dactylus strongly convex; endopod 1.2 times as long as wide, lateral slender, 3.8 as long as propodus, 3.8 times as long margin convex, distally broadly rounded, medial margin as basal width. Pereopods 3–6 similar to pereopod 2, straight; peduncle 0.3 times as wide as long. Pleopods gradually increasing in size towards posterior, all without 2–5 similar to pleopod 1. Pleopods 3–5 with fleshy folds setae. Pereopod 7 basis 0.6 times as long as greatest present, increasing in size from pleopod 3–5. Peduncle width; ischium 0.8 as long as basis, without protrusions; lobes present, increasing in size from pleopod 1–5. Figure 3: Norileca indica (Milne Edwards, 1840) ovigerous female (33.0 mm TL, 16.0 mm W) (SAMC-A089028). (a) Ventral cephalon, (b) oostegites, (c) pereopod 1, (d) pereopod 7 168 van der Wal, Smit and Hadfield Figure 4: Norileca indica (Milne Edwards, 1840) ovigerous female (33.0 mm TL, 16.0 mm W) (SAMC-A089028). (a) Pleopod 1 dorsal view, (b) pleopod 2 dorsal view, (c) pleopod 3 dorsal view, (d) pleopod 4 dorsal view, (e) pleopod 5 dorsal view, (f) pleopod 1 ventral view, (g) pleopod 2 ventral view, (h) pleopod 3 ventral view, (i) pleopod 4 ventral view, (j) pleopod 5 ventral view African Zoology 2017, 52(3): 163–175 169 Uropod more than half the length of pleotelson; peduncle eyes. Posterior margins of pereonites smooth and straight. 0.7 times longer than rami, lateral margin without setae; rami Coxae 2–3 wide; with posteroventral angles rounded; not extending beyond pleotelson, marginal setae absent, 4–7 acute, posteriorly pointed; not extending past pereonite apices narrowly rounded. Endopod 2.3 times as long as margin. Pereonites 6 and 7 becoming more progressively greatest width, without setae. Exopod not extending to end rounded posteriorly. Pleon with pleonite 1 largely concealed of endopod, 3 times as long as greatest width, without setae. by pereonite 7; pleonites posterior margin smooth, mostly concave. Pleonite 2 not overlapped by pereonite 7; postero- Male lateral angles of pleonite 2 rounded. Pleonites 3–5 similar (Figures 5–7) in form to pleonite 2; pleonite 5 free, not overlapped by lateral margins of pleonite 4. Pleotelson as long as anterior Length 11.0 mm, width 3.0 mm. width; dorsal surface smooth; lateral margins weakly Body straight, not twisted, 2.7 times as long as greatest convex, posterior margin converging to caudomedial point. width, widest at pereonite 5, most narrow at pereonite Antennula more stout than antenna, longer than antenna; 1, pereonite lateral margins mostly posteriorly ovate. consists of 8 articles; peduncle articles 1 and 2 distinct and Cephalon 0.79 times longer than wide, visible from dorsal articulated; article 2 as long as article 1; article 3 1.4 times view, triangular, not immersed in pereonite 1. Frontal as long as wide, 0.5 times as long as combined lengths margin thickened, ventrally folded. Eyes oval with distinct of articles 1 and 2; flagellum with 5 articles, extending to margins; one eye 0.6 times length of cephalon. Pereonite anterior of pereonite 1, with tufts of setae on articles 3–8. 1 smooth, anterior border indented; anterolateral angle Antenna consists of 9 articles; peduncle article 3 1.1 times weakly produced, extending past the posterior margin of as long as article 2; article 4 1.5 times as long as wide, Figure 5: Norileca indica (Milne Edwards, 1840) male (11.0 mm TL, 3.0 mm W) (SAMC-A089028). (a) Dorsal body, (b) lateral body, (c) dorsal view of cephalon and pereonite 1, (d) dorsal view of pleotelson with uropods, (e) penes 170 van der Wal, Smit and Hadfield Figure 6: Norileca indica (Milne Edwards, 1840) male (11.0 mm TL, 3.0 mm W) (SAMC-A089028). (a) Antenna, (b) antennula, (c) pereopod 1, (d) pereopod 7, (e) mandibular palp, (f) maxilliped, (g) tip of maxillule, (h) maxilla African Zoology 2017, 52(3): 163–175 171 1.3 times as long as article 3; article 5 1.6 times as long as paper presents the first report of N. indica from Maputo wide, as long as article 4. Antenna flagellum with 7 articles, Bay, Mozambique, representing the most southern distri- terminal article terminating in 1–5 short simple setae, bution in the Indian Ocean for this species. From the distri- extending to anterior margin of pereonite 1. Mandibular bution data, it is evident that most N. indica recordings molar process present; palp article 2 with 3 distolateral have been made from the eastern regions of the Indian setae, article 3 with 6 simple setae. Maxillule simple with Ocean. The localities from this study, as well as from Trilles 4 terminal robust setae. Maxilla medial lobe not fused to (1976) and Rokicki (1982), provide the only evidence of the lateral lobe; medial lobe with 2 recurved robust setae, presence of N. indica from the western region of the Indian lateral lobe with 1 large recurved robust setae. Maxilliped Ocean. Records of N. indica correspond to the distribution consists of 3 articles; palp article 2 without setae; article 3 pattern of their fish hosts. with 4 recurved robust setae. Pereopod 1 basis 1.7 times as long as greatest width; Hosts ischium 0.6 times as long as basis; merus proximal Hosts are usually pelagic and demersal marine teleosts margin with slight bulbous protrusion; carpus with rounded with a preference towards schooling fish, especially those proximal margin; propodus 1.3 times as long as wide; from the family Carangidae. Hosts include smallmouth dactylus slender, 1.8 as long as propodus, 3.8 times as scad, Alepes apercna Grant, 1987 (see Trilles 1976); long as basal width. Pereopod 7 basis 1.6 times as long Indian mackerel, Rastelliger kanagurta Cuvier, 1816 (see as greatest width; ischium 0.9 as long as basis, without Avdeev 1978; Rokicki 1982; Ghani 2003; Rameshkumar protrusions; merus proximal margin with slight bulbous et al. 2015); blackfin scad, Alepes melanoptera Swainson, protrusion, 0.6 times as long as wide, 0.3 as long as 1839 (previously as Atule malam Bleeker, 1851) (see ischium; carpus 0.6 times as long as wide, 0.2 as long as Avdeev 1978); bigeye scad Selar crumenophthalmus ischium, without bulbous protrusion; propodus 1.4 times Bloch, 1793 (see Rokicki 1982; Bruce 1990; Nagasawa and as long as wide, 0.5 as long as ischium; dactylus slender, Petchsupa 2009; Neeraja et al. 2014; Cruz-Lacierda and 1.7 as long as propodus, 3.6 times as long as basal width. Nagasawa 2017; present study); Herklotsichthys sp. (see Pleopod exopod larger than endopod. Pleopod 1 exopod Bruce 1990; Ghani 2003; Yu and Li 2003); and Decapterus 1.3 times as long as wide, lateral margin weakly convex, sp. including the Indian scad, D. russelli Ruppell, 1830 distally narrowly rounded, medial margin weakly oblique; (see Ghani 2003). Other recent host records include the endopod 1.6 times as long as wide, lateral margin slightly pugnose ponyfish, Secutor insidiator Bloch, 1787 (see straight, distally narrowly rounded, medial margin straight; Behera et al. 2016), and the redtail scad Decapterus peduncle 0.3 times as wide as long, without retinaculae. kurroides Bleeker, 1855 (see Cruz-Lacierda and Nagasawa Pleopod 2 appendix masculina with parallel margins, 2017). Yamauchi et al. (2005) obtained N. indica from the 0.8 times as long as endopod, distally acute. Pleopod 5 stomach of the common dolphinfish, Coryphaena hippurus with fleshy folds present. Peduncle lobes present, Linnaeus, 1758 where the natural host would have been increasing in size from pleopod 1 to 5. eaten by the dolphinfish. Uropod same length as pleotelson, peduncle 0.8 times Behera et al. (2016) recorded N. indica from Randall’s longer than rami, peduncle lateral margin without setae; threadfin bream, Nemipterus randalli Russell, 1986, which rami extending to pleotelson apex, marginal setae absent, is a doubtful host record. It is the first and only host record apices narrowly rounded. 2.5 times as long as greatest from the family Nemipteridae and a photograph provided width, without setae. Exopod 2.4 times as long as greatest by Behera et al. (2016: see fig. 5c) does not represent width, without setae. N. indica. Penes prominent, 2.3 times as long as basal width, tubercules connecting at base. Molecular characterisation Two ovigerous females were sequenced (forward and Distribution reverse). Ovigerous female (30.0 mm TL, 17 mm W) Off the Zambezi estuary, Mozambique and Tanjona produced a 686 bp contig of the COI gene (accession Vilanandro, north-western coast of Madagascar (previously number: MF628258), and ovigerous female (26.0 mm TL, Cape Saint André) (Rokicki 1982); Mayotte Island (Trilles 13 mm W) produced a 687 bp and 679 bp contig of the COI 1976); Pakistan (Behera et al. 2016); India (Rameshkumar gene (accession numbers: MF628259 and MF628260), et al. 2013b, 2015) as well as Indian eastern coast and respectively. These COI gene sequences are the first Visakhapatnam (north-west Bay of Bengal) (Behera et al. sequences to be generated for N. indica and the genus 2016); Thailand (Nagasawa and Petchsupa 2009) and Ko Norileca, therefore species validity and generic placement Khram (Schioedte and Meinert 1884); Indonesia (Milne based on molecular evidence could not be done. Edwards 1840; Trilles 1979); China (Yu and Li 2003); Mariveles and Luzon Islands (Schioedte and Meinert Remarks 1884; Trilles 1976; Yamauchi et al. 2005) and Panay Norileca indica attaches to the ventral part of the host Gulf, Province of Iloilo, the Philippines (Cruz-Lacierda and branchial cavity, with the cephalon to the anterior end of Nagasawa 2017); Arafura Sea, off the Northern Territory the host, and with its ventral side (abdomen/brood pouch) coast of Australia (Bruce 1990); and north-western directed outwards, facing the branchial operculum (Bruce Australia (Avdeev 1978). 1990; Neeraja et al. 2014; Rameshkumar et al. 2015; The only previous record of N. indica from Mozambique Behera et al. 2016). Its asymmetrical body is twisted was by Rokicki (1982), off the Zambezi river estuary. This to the left when it occupies the right branchial cavity and Figure 7: Norileca indica (Milne Edwards, 1840) male (11.0 mm TL, 3.0 mm W) (SAMC-A089028). (a) Pleopod 1 dorsal view, (b) pleopod 2 dorsal view, (c) pleopod 3 dorsal view, (d) pleopod 4 dorsal view, (e) pleopod 5 dorsal view, (f) pleopod 1 ventral view, (g) pleopod 2 ventral view, (h) pleopod 3 ventral view, (i) pleopod 4 ventral view, (j) pleopod 5 ventral view African Zoology 2017, 52(3): 163–175 173 twisted to the right when it occupies the left branchial cavity Cymothoid isopods are protandrous hermaphorodites, (Nagasawa and Petchsupa 2009; Neeraja et al. 2014). making them difficult to identify during different develop- Norileca indica can be recognised by its twisted body, with mental stages. As part of the female development, the a 2.1–2.5 length-to-width body ratio and the oval eyes have pleotelson becomes wider and other structures (such as the distinct margins. The pleotelson of N. indica is approxi- gonopod, eye- and uropod perimeter, and the first antenna) mately as long as it is wide and the uropods are two-thirds become shorter in length (Cook and Munguia 2015). Males the length of the pleotelson length. Furthermore, pleonite 5 tend to be morphologically similar to one another; therefore, is about as wide as pleonite 1. accurate and comprehensive descriptions of males are Males are similar in appearance to females but smaller essential to ensure species identification can potentially be in size and with a straight body shape. Ovigerous females made in the absence of ovigerous females. differ from non-ovigerous females in having a larger Norileca indica is widely distributed and morphological body length-to-width ratio as they become wider as eggs analyses combined with molecular analyses will provide develop in the broodpouch. Both Rokicki (1982) and a better understanding of this species. These analyses will Bruce (1990) reported that N. indica is ventrally positioned confirm species identity, even during the natatory stage in the host gill cavity with the cephalon facing the anterior of development (see Jones et al. 2008). It is essential to end of the host and the abdomen outwards toward the combine genetic characterisation of a species with an operculum (in a lateral position). Four of the currently accompanying description of that species based on the same collected specimens were also ventrally positioned; material in order to verify the identification of the species. however, two were positioned with the dorsal surface Only when the identification of the species is accurate to the operculum. can phylogenetic analysis be effective, providing useful Norileca indica can be distinguished from N. triangu- information without having the confusion of misidentified lata by being larger than the latter, with its body twisted species as is currently the problem with cymothoids. to the side, a straight sided pleon, smaller eyes, as well The use of combined molecular and morphological as shorter uropods and a shorter mandible palp article 3 data for phylogenetics is becoming more prominent (Bruce 1990). It differs from N. borealis by having shorter within taxonomic publications. This combination improves uropods, larger eyes, and a larger length-to-width ratio the resolution, internal support and overall quality of of the pleotelson. Pleonite 1 and 5 of N. indica are more phylogenetic studies (Caddick et al. 2002; Scotland et equal in width than that of N. borealis where pleonite 5 al. 2003). In many instances, there exists a lack of either is narrower than pleonite 1. In addition, N. borealis has a morphological or molecular data (Giribet et al. 2001). This medial lobe with 4 recurved robust setae (two recurved is also the case with N. indica, as no other publication is robust setae on N. indica), and article 3 of the maxilliped available that provides a comprehensive data set of both with three recurved robust setae (4 recurved robust setae morphological and molecular results of this species. The on N. indica) (Javed and Yasmeen 1999). Even though use of molecular techniques seems to eliminate morpho- N. borealis and N. triangulata are more similar to each logical bias as well as over- and under-estimations of other than to N. indica, they can be distinguished from each biodiversity that is occasionally associated with traditional other by body shape, ventral margin of the cephalon, as morphological analyses (Lefébure et al. 2006). well as pleon and pleopod morphology. The first molecular characterisation of N. indica presented Since the redescription of N. indica in 1990, records here contributes to the limited pool of molecular information of this species from the Indian subcontinent have mainly of the Cymothoidae (currently only 28 of the 385 known and been made due to the collection of its fish hosts for accepted cymothoid species have been sequenced), while subsistence and commercial use by local fisherman. Many also providing a Norileca COI sequence that can be used of its host species, including Selar crumenophthalmus and for cymothoid studies as well as species identifications. Decapterus kurroides, are considered to be commercially Acknowledgements — The project was funded through a Western important fish species (Argente et al. 2014; Cruz-Lacierda Indian Ocean Marine Science Association (WIOMSA) Marine and Nagasawa 2017). Other publications from this region Research Grant as well as a Claude Leon Foundation postdoctoral provided new host or locality information on N. indica fellowship for KA Hadfield. The financial assistance of the National as well as some ecological data including prevalence, Research Foundation (NRF) (NRF project IFR170210222411 grant mean intensity and abundance (Neeraja et al. 2014; 109352, NJ Smit, PI) and the Foundational Biodiversity Information Rameshkumar et al 2015; Behera et al. 2016; Jithin et Programme (DST-NRF FBIP, UID: 108783, S van der Wal) is al. 2016). Despite this species being frequently collected, hereby acknowledged. Opinions expressed, and conclusions arrived at, are those of the authors and are not necessarily those limited work has been done recently on the morphology of the NRF. The authors would like to thank Wynand Vlok for and taxonomy of this species. assistance in collecting the isopods. This is contribution number 213 from the NWU-Water Research Group. Discussion References The redescription of N. indica by Bruce (1990) was based on non-ovigerous females. 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