Systematic Parasitology

, Volume 72, Issue 2, pp 97–112

Gnathia trimaculata n. sp. (Crustacea: Isopoda: Gnathiidae), an ectoparasite found parasitising requiem sharks from off Lizard Island, Great Barrier Reef, Australia

Authors

  • Maryke L. Coetzee
    • Department of ZoologyUniversity of Johannesburg
    • Department of ZoologyUniversity of Johannesburg
  • Alexandra S. Grutter
    • School of Integrative BiologyThe University of Queensland
  • Angela J. Davies
    • Department of ZoologyUniversity of Johannesburg
    • School of Life Sciences, Faculty of ScienceKingston University
Article

DOI: 10.1007/s11230-008-9158-2

Cite this article as:
Coetzee, M.L., Smit, N.J., Grutter, A.S. et al. Syst Parasitol (2009) 72: 97. doi:10.1007/s11230-008-9158-2

Abstract

Gnathia trimaculata n. sp. is described from one black tip reef shark Carcharinus melanopterus Quoy & Gaimard and four grey reef sharks C. amblyrhynchos Bleeker collected off Lizard Island, Great Barrier Reef, Australia. Third-stage juveniles (praniza 3) were maintained in fresh seawater until they moulted into adults. Male adults emerged seven days post-removal (d.p.r) of pranizae from host fishes, whereas the female pranizae completed their moult into adult females 24 d.p.r. Distinctive features include the relatively large size of all stages and the unique mediofrontal process of the male, which is divided into two lobes forming a key-hole shape between them. The female frontal border is characterised by paired simple, pappose setae on the sides of the mid-dorsal area, as well as four long, pappose setae on the mid-dorsal region. The pranizae have eight teeth on each mandible. Live pranizae have stripes and three pairs of distinctive black spots within yellow circles on the sides of the pereonites and this pigmentation pattern persists in the adults. This represents the second description of a gnathiid parasitising elasmobranchs off Australia.

Introduction

Members of the isopod family Gnathiidae Leach, 1814 demonstrate protelian parasitism; thus only the juvenile (larval) stages are parasitic, while reproductive adults are free-living (Smit & Davies, 2004). Smit & Davies (2004) listed 173 species of gnathiids in ten genera, and two new genera (Tanaka, 2005; Hadfield & Smit, 2008) and seven new species (Nunomura & Honma, 2004; Svavarsson & Jörundsdóttir, 2004; Tanaka, 2005; Svavarsson, 2006; Coetzee et al., 2008; Hadfield & Smit, 2008) have since been recorded. Of the current total of 180 species, 46 have been reported from Australian waters, 14 from off Queensland and six of these from the Great Barrier Reef (GBR). Grutter (1994) demonstrated that gnathiid larvae are among the most common teleost fish ectoparasites on the GBR. They have been reported to parasitise elasmobranchs, in some cases in high abundance exceeding 200 per host on Heron Island (Grutter & Poulin, 1998). Heupel & Bennet (1999) showed a positive correlation between their numbers and fish size for the epaulette shark Hemiscyllium ocellatum Bonnaterre, but concluded that the parasites did not cause significant tissue damage. McKiernan et al. (2005) also reported on the ecology of gnathiids attached to epaulette sharks on the GBR. The gnathiids studied in the above investigations were identified to generic level, but none to species level and currently only three have been described parasitising elasmobranchs: Gnathia pantherina Smit & Basson, 2002 from South African sharks and rays, Poroderma pantherinum Smith, Haploblepharus edwardsii Voight and Torpedo fuscomaculata Peters; G. capillata Nunomura & Honma, 2004 from Japanese rays and sharks, Dasyatis akajei Müller & Henle, D. matsubarai Miyosi and Mustelus manazo Bleeker; and G. grandilaris Coetzee, Smit, Grutter & Davies, 2008 from Australian requiem sharks, Carcharhinus amblyrhynchos Bleeker and Triaenodon obesus Rüppell. This paper reports on a new species of gnathiid also parasitising requiem sharks, the black tip reef shark C. melanopterus Quoy & Gaimard and grey reef shark C. amblyrhynchos.

Materials and methods

During March 2002, a single black tip reef shark (TL 1118 mm) and four grey reef sharks, ranging in length from 920–1,464 mm (mean ± S.E., 1,393.5 ± 331.5 mm) were captured by rod and line as part of an ongoing study by James Cook University on shark age (Great Barrier Reef Marine Park Authority, GBRMPA permit G02/021). Collection methods for sharks and gnathiids followed Coetzee et al. (2008). FishBase was used to identify authorities of all hosts collected (Froese & Pauly, 2008). Of nine juvenile gnathiids collected from the black tip reef shark, six were allowed to moult to adults at 24–27°C, and, of 57 juveniles from four grey reef sharks, 46 were moulted to adults at the same temperature. Of the 46 moulted juveniles, 25 became males, 11 females and ten died before they could complete their moult. Males and females were then paired to determine whether fertilisation could occur. After the successful fertilisation of females and the development of first-stage juveniles, both males and females were fixed in 70% ethanol. For brightfield microscopy, specimens were stained in lignin pink for 24 hours and cleared in lactic acid before drawing each stage for taxonomic purposes. Specimens were also prepared for scanning electron microscopy following the techniques described by Smit & Van As (2002) and Coetzee et al. (2008). The anatomical terminology, as well as the numbering of pereonites and pereopods, used by Cohen & Poore (1994) and the setal classification used by Watling (1989) and Garm (2004) were applied.

Results

All five reef sharks examined had gnathiid juveniles present on their gill septum and filaments. The number of gnathiids varied from nine on the black tip to 32 on one of the grey reef sharks. All juveniles collected had fed and were seemingly in their third (praniza 3) stage, since those that moulted became adults. Male larvae moulted to adult males at six days post removal (d.p.r.) from shark gills, completing this process seven d.p.r. The moulting process followed the same pattern described for Gnathia grandilaris by Coetzee et al. (2008). Female larvae moulted to adults from 20 d.p.r., completing this transition by 24 d.p.r. Males were able to fertilise females, the eggs developing into first-stage (zuphea 1) larvae, thus confirming that the males, females and juveniles all belonged to the same species.

Gnathia trimaculata n. sp.

Type-host: Carcharinus melanopterus Quoy & Gaimard.

Other host: C. amblyrhynchos Bleeker.

Type-locality: Off Lizard Island (14°40′54.68″S, 145°26′53.72″E), Australia. Hosts collected by Will Robins (James Cook University) and Tom Lisney (The University of Queensland); parasites collected by N.J. Smit.

Type-material: Holotype: in the collection of the Queensland Museum, Brisbane, Australia (male) (W28386). Paratypes: (four males, three females and three pranizae) (W28387), in the same collection. Other material in the collection of one of us (NJS), Department of Zoology, University of Johannesburg.

Attachment site: Juveniles attached to gill filaments and septum.

Etymology: The specific epithet is adjectival and derived from the Latin combination of ‘tri’ and ‘maculata’, meaning three-spotted, referring to the distinctive three pairs of spots on the pereon of all stages, and most pronounced in the juveniles.

Description

Male (Figs. 1A–H; 2A–C; 3A; 10A,B; 11A)
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Fig. 1

Gnathia trimaculata n. sp., male (W28386). A Full length dorsal view; B Frontal border and mandibles; C Lateral view of cephalosome; D First antenna; E Second antenna; F Dorsal view of mandible; G Pleotelson and uropods; H Left pleopod 2 with appendix masculina. Scale-bars: A, 1 mm; B,C, 500 μm; DH, 100 μm

Size. Total length of holotype: 4.4 mm. Total length of paratypes: 4.0–5.4 mm (4.5 ± 0.7 mm, n = 7).

Cephalosome. Rectangular, 1.6 times as wide as long, with deep dorsal sulcus, narrower than width of median process, extending 1/3 length of cephalosome (Fig. 1A); lateral margins convex; row of long pappose setae and tubercles extend laterally from under eyes posterio-medially, not reaching median tubercle; posterior margin concave (Fig. 1A). Sensory pits, some with single short pappose seta, and short hair-like simple setae distributed randomly over dorsal and lateral surface of cephalosome; sensory pits present in dorsal sulcus. Small wart-like tubercles distributed randomly over dorsal surface (Fig. 1A,B). Pappose setae, sensory pits and short simple setae ventrally on lateral sides of buccal cavity. Well-developed oval-shaped, bulbous, sessile compound eyes on lateral margin of cephalosome; length of eye slightly less than 1/3 of cephalosome. Eight to 10 paraocular tubercles with long pappose setae (Fig. 1C). Elliptical posterior median tubercle present.

Frontal border. Produced superior frontolateral process absent. Mediofrontal process divided into 2 lobes almost touching anteriorly forming distinct key-hole shape. Four to 5 pairs of long pappose setae present ventrally on both lobes (Fig. 1A,B). Row of 4–6 pappose setae run anterior-posterior on each lobe (Fig. 1B). Lamina dentata with 7–9 tubercles visible. External scissura shallow. Supraocular lobe pronounced with 7–9 pappose setae and 4–6 tubercles dorsally.

Antennae. Three peduncle articles of antenna 1 covered with very short hair-like simple setae (Fig. 1D). Flagellum with 5 articles; article 3 largest; articles 3 and 4 with single aesthetasc seta each; article 5 terminates in 1 aesthetasc and 3 simple setae; few setae on each article. Antenna 2 peduncle covered with very short hair-like simple setae; flagellum with 7 articles; article 7 terminates in 5 simple setae. Articles 2–6 of flagellum with 1–2 simple setae on anterior end (Fig. 1E).
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Fig. 2

Cephalosome appendages of a male Gnathia trimaculata n. sp. (W28386). A Maxilliped; B Pylopod; C Articles 2 and 3 of pylopod. Scale-bars: 100 μm

Mandible. One-third length of cephalosome, 2.3 times longer than wide, with broad basal neck, curved inwards with 7–8 processes on dentate blade and cluster of setae between processes (Fig. 1F). Apex cylindrical, raised distally in lateral view. Slight incisor present. Single pappose mandibular seta extending from base of incisor process. Carina armed, forms ridge on lateral margin extends from basal neck to 1/3 length of mandible. Short simple hair-like setae distributed randomly on dorsal surface of blade. Internal lobe and pseudoblade absent.

Maxilliped. Proximal article largest with slender mediodistal endite reaching article 3 (Fig. 2A). Lateral margin, and posterior margin, of proximal article densely setose. Distal 4 articles bear plumose setae on lateral margins in order 5-7-5-8; mesial border with short simple setae. Single simple seta on anterior lateral side of articles 2 and 4. Palp 1.9 times as long as wide. No coupling hooks.

Pylopod. Twice as long as broad, with 3 articles. First article mesial border convex, fringed with 31 similar-sized plumose setae; lateral and proximal setae short and simple; 2 plumose and 7 simple setae near mid-lateral border, plus single simple seta distally on posterior surface (Fig. 2B). Second article oval, 1.3 times as long as wide; margins setose; 11 simple setae distally on posterior surface. Third article minute, with fringing setae (Fig. 2C). Large single areola present; dorsal surface covered with short hair-like simple setae.

Pereon. Longer than wide (1.8 times), wider than cephalosome, covered with numerous long pappose setae and short simple hair-like setae. Pereonite 1 visible dorsally, not reaching lateral margins; anterior border convex; posterior margin slightly concave (Fig. 1A). Pereonites 2 and 3 of similar size; tubercles present on pereonite 3. Pereonite 4 with prominent anterior constriction separating it from pereonite 3. Tubercles and long pappose setae on anterior and posterior lateral lobes of pereonite 4; median groove present. Pereonite 5 with areae laterales and dorsal sulcus in form of thin groove. Pereonite 5 widest part of body. Pereonites 5 and 6 not fused. Pereonite 6 at least twice as long as pereonites 1, 2 and 4, and slightly longer than pereonite 5. Pereonite 6 longer than wide (1.6 times); posterior margin deeply concave, with lobi laterales and no lobuii; setae present on lateral lobes, as well as on mid-posterior concave margin. Pereonite 7 visible dorsally, small, with rounded posterior margin, overlaps first pleonite.

Pleon. Pleon and pleotelson less than 1/3 of total length (Figs. 1A, 11A). Pleonites with prominent epimera visible dorsally and long pappose setae specifically distributed on lateral sides.

Pleotelson. Longer than wide; lateral margins concave; dorsal surface with 4 pairs of long pappose setae and many pectinate scales; distal apex terminates in pair of long pappose setae (Fig. 1G).
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Fig. 3

Pereopods 2 to 6 (P2–P6) of a male Gnathia trimaculata n. sp. (W28386). Scale-bar: 200 μm

Pereopods. Pereopod 2 (Fig. 3A) basis sub-quadrate, with single simple seta and 5 plumose setae anteriorly and 9 pappose setae posteriorly. Ischium 2/3 length of basis, with 3 anterior setae and 6 posterior pappose setae. Merus 1/2 length of ischium, with anterior bulbous protrusion, 2 simple setae on bulbous protrusion and 2 plumose setae present anteriorly; posterior margin with 4 plumose setae. Carpus almost same size and shape as merus, but without anterior bulbous protrusion, with 4 pappose and single simple seta present posteriorly and 2 pappose setae and single simple seta present anteriorly. Dactylus 1/2 length of propodus, terminates in sharp posteriorly oriented unguis. Posterior margin with 2 pappose setae. Propodus twice length of carpus, with 2 robust denticulate setae situated on middle and anterior end. Pereopods 3–6, somewhat similar to pereopod 2, differing in setation and distribution of tubercles. Pereopod 3 with distinct tooth-shaped tubercles on anterior margin of basis and posterior margin of carpus. Pereopod 4 with 2 distinct tooth-shaped tubercles on posterior margin of basis and single tooth-shaped tubercles on anterior margin of ischium, merus and carpus. Pereopod 6 with 2 robust elongate serrate setae on posterior bulbous protrusion of merus. Dorsal surface of all pereopods covered with pectinate scales (drawn only for P6; Fig. 3A).

Pleopod. Exopod fringed distally with 7 short pappose setae; short pappose seta on lateral and posterior margins of sympodite. Sympodite with retinaculae on medial margin. Two short simple setae present on distal margin of endopod. All pleopods similar, except pleopod 2 with appendix masculina attached to mesial junction between endopod and sympodite; appendix masculina 2/3 length of endopod (Fig. 1H).

Uropod. Rami extending beyond apex of pleotelson; endopod with 8 long pappose setae on distal margin and single pappose seta on lateral margin; exopod with 5 long pappose setae on lateral margin and 7 long pappose setae distally; pectinate scales on lateral, dorsal and anterior surfaces of uropods (Fig. 1G). Single pappose seta present on uropodal basis.

Penis. Prominent, with 2 contiguous papillae, wider than long, ventral on pereonite 6. Two pairs of simple short setae distal to penis.

Live specimens. Light brown pigmentation between eyes on antero-dorsal surface of cephalosome. Pereonites 5 and 6 with yellow and brown pigmentation, with 3 distinct black stripes dorsally reaching from anterior constriction of pereonite 5 almost to posterior end of pereonite 6 (Fig. 11A). Three pairs of brown spots occur laterally on pereon.

Female (Figs. 4A-F; 5A, B; 6A; 10C; 11B)

Size. Total length of paratypes: 4.0–4.3 mm (4.1 ± 0.1 mm, n = 3).

Cephalosome. Short, rectangular, 1.2 times as wide as long; short simple seta on dorsal, lateral and ventral cephalosome; posterior margin straight (Figs. 4A, 10C). Well-developed oval bulbous compound eyes on lateral margin of cephalosome; length of eye 3/4 of cephalosome. No paraocular ornamentation, only 4 short pappose setae (Fig. 4B). Elliptical postero-median tubercle, plus single pair of simple setae and pair of pappose setae on lateral sides of tubercle.
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Fig. 4

Gnathia trimaculata n. sp., female (W28387). A Full length dorsal view; B Cephalosome and frontal border; C First antenna; D Second antenna; E Pleotelson and uropods; F Left pleopod 2. Scale-bars: A, 1 mm; B, 10 μm; CF, 100 μm

Frontal border. Broadly rounded, produced, slightly concave anteriorly, with pair of simple pappose setae on sides of mid-dorsal area, plus 4 long pappose setae on mid-dorsal region (Fig. 4A).

Antennae. Antenna 1 (Fig. 4C) with 3 peduncle articles, increasing in length distally, with 3rd article longest; single plumose setae present on article 1 and pair of simple setae on article 2; flagellum with 5 articles; article 2 largest; articles 3 and 4 with single aesthetasc seta each; article 5 terminates in single aesthetasc and 3 simple setae. Antenna 2 (Fig. 4D) with 5 peduncle articles; article 5 largest; 4 long pappose setae on distal end of articles; flagellum with 7 articles; article 1 largest; article 7 terminates in 3 simple setae; articles 2–6 of flagellum with 1–2 simple setae on anterior end. Peduncle articles of both antennae covered with very short simple hair-like setae. Pectinate scales present only on article 3 of antenna 1 and articles 4 and 5 of antenna 2.

Maxilliped. Consists of coxa with attached oöstegite, basis and palp of 4 articles (Fig. 5A). Endite short, not reaching article 2 of palp. Lateral margins of basis fringed. Palp bearing plumose setae on lateral margins in order of 4-6-5-7. Mesial borders of basis, palp and oöstegite densely setose.
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Fig. 5

Cephalosome appendages of a female Gnathia trimaculata n. sp. (W28387). A Right maxilliped; B Left pylopod. Scale-bar: 100 μm

Pylopod. Comprises 3 articles; articles 1 and 2 fused. Article 1 broad, robust, curved anteriorly; article 2 with single short pappose seta laterally. Article 3 with 8 long pappose setae distally and 2 simple short setae on lateral side (Fig. 5B). Oöstegite oval, 1.7 times broader than long, covers mouthparts ventrally but does not surpass frontal border. Posterior surface of article 2 and proximal and distal halves of article 1 covered with pectinate scales. Lateral borders of all articles and oöstegite covered with short simple hair-like setae.

Pereon. Swollen round, with sutures between pereonites 5–7, 1.3 times as long as wide, wider than cephalosome (Figs. 4A, 11B), covered with numerous long pappose setae and short simple hair-like setae. Pereonite 7 visible dorsally, small, with rounded posterior margin, overlaps first pleonite. Setae on anterior and lateral margins of all pereonites.

Pleon. Pleon and pleotelson less than 1/4 of total length (Fig. 4A). Five subequal pleonites visible dorsally; epimera not distinct; short hair-like setae and short pappose setae randomly distributed on pleonites.

Pleotelson. Triangular; base wider than length; lateral margins concave; dorsal surface with 3 pairs of plumose setae and pectinate scales; distal apex terminates in pair of long pappose setae (Fig. 4E).

Pereopods. Pereopod 2 basis subquadrate with single pappose seta anteriorly, 4 plumose setae and 1 simple seta posteriorly (Fig. 6A). Ischium 2/3 length of basis, with 2 plumose setae plus 2 simple setae anteriorly and 6 simple plumose setae posteriorly. Merus 1/2 length of ischium, with anterior bulbous protrusion bearing 1 simple seta and 2 pappose setae anteriorly; posterior margin with 2 pappose setae and 2 simple setae. Carpus almost same size and shape as merus, but without anterior bulbous protrusion; 2 pappose setae posteriorly and single simple seta anteriorly. Propodus about twice length of carpus, with 2 plumose setae on anterior side and 2 simple setae on posterior half of propodus. Two robust denticulate setae present distally on propodus. Dactylus 1/2 length of propodus, terminates in sharp posteriorly oriented unguis; robust seta on posterior side proximal to unguis and with few simple setae on dorsal and ventral sides of robust seta. Margins of all articles densely setose. Pereopods 3–6 similar to pereopod 2 in basic form, differing in setation, shape and number of tubercles (Fig. 6A). Pereopod 3 with single tooth-shaped tubercle anteriorly on basis and 2 posteriorly on carpus. Pereopod 4 with single tooth-shaped tubercle on posterior side of carpus. Pereopod 6 with 2 elongate robust serrate setae on posterior bulbous protrusion of merus. Dorsal surface of all pereopods covered with pectinate scales. Coxae of pereopods 4–6 with thin overlapping plate-like oöstegites enclosing brood pouch.
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Fig. 6

Pereopods 2 to 6 (P2–P6) of a female Gnathia trimaculata n. sp. (W28387). Scale-bar: 200 μm

Pleopod. Endopod fringed distally with 1 short pappose seta and exopod with 8 short pappose setae (Fig. 4F). Sympodite with retinaculae on mesial border. Pleopods 2–5 similar to pleopod 1.

Uropod. Rami extend beyond apex of pleotelson; endopod longer and wider than exopod. Endopod with 8 long pappose distal setae and single lateral pappose seta; exopod with 5 long distal pappose setae and 4 lateral pappose setae (Fig. 4F). Pectinate scales on antero-lateral areas of uropods. Uropodal basis with single plumose seta.

Live specimens. Female generally yellow with dark half-moon-shaped pigmentation on dorsal cephalosome and 3 black pigment stripes on dorsal surface of pereonites 4, 5 and 6, extending onto pleon and almost reaching pleotelson (Fig. 11B). Three pairs of dark spots on lateral sides of pereon.

Third-stage praniza (Figs. 7A–F; 8A–E; 9A; 10D; 11C,D)

Size. Total length of paratypes: 2.5–5.3 mm (4.0 ± 1.1 mm, n = 8).

Cephalosome. Posterior margin straight, slightly wider than anterior margin, almost as wide as long; lateral margins slightly convex (Figs. 7A, 11C). Many sensory pits and pair of short simple setae on dorsal surface of cephalosome. Compound eyes large, well developed, oval, bulbous, on lateral margins of cephalosome; length of eye almost same as cephalosome. No sulci or tubercles on dorsal cephalosome. Antero-medial margin of cephalosome straight, with deep lateral concave excavations to accommodate first articles of antennae.
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Fig. 7

Gnathia trimaculata n. sp., third-stage praniza larva (W28387). A Full length dorsal view; B Dorsal cephalosome with labrum and antennae; C Antenna one; D Antenna two; E Pleotelson and uropods; F Right pleopod 2. Scale-bars: A, 1 mm; B, 500 μm; C,D, 100 μm; E,F, 200 μm

Labrum. Prominent, 1/2 length of cephalosome, semicircular with apical process; truncate posterior margin; anterior margin concave (Figs. 7B, 11C). Ventral part of labrum gutter-like, with central groove covering mandibles dorsally and laterally.

Antennae. Antenna 1 with 3 peduncle articles; article 3 largest, with pectinate scales forming row on anterior border and 4 simple setae distally (Fig. 7C); flagellum with 4 articles; first article with no setae; article 2 largest; articles 2 and 3 with 1 aesthetasc seta each; article 4 terminates in 1 aesthetasc and 3 simple setae. Antenna 2 article 1 with single simple setae anteriorly; article 2 with 4 simple setae anteriorly; article 3 with single simple setae anteriorly; article 4 largest; flagellum with 7 articles; article 7 terminates in 3 simple setae (Fig. 7D).

Mandible. Stout, swollen at base; distal margin styliform with 8 teeth on mesial margin; teeth triangular and backwardly directed, increasing in size from anterior to posterior (Fig. 8A).
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Fig. 8

Cephalosome appendages of a praniza larva of a Gnathia trimaculata n. sp. (W28387). A. Mandible; B Paragnath; C Maxillule; D Maxilliped; E Gnathopod. Scale-bars: AD, 100 μm; E, 10 μm

Paragnaths. Elongate, gutter-like, terminate in sharp point; teeth and setae absent (Fig. 8B).

Maxillule. Long, slender (Fig. 8C), with swollen base, reaching past distal margin of labrum. Seven small teeth on distal inner margin.

Maxilliped. Large, cylindrical, elongate base, with pectinate scales and short hair-like setae laterally; endite almost reaches palp, with single long simple seta. Palp with 3 articles; first article acute, with 3–4 small teeth and single simple seta medially; article 3 with 4 simple setae (Fig. 8D).

Gnathopod. Smaller than pereopods, with 7 articles; few simple setae distributed randomly on articles (Fig. 8E). Pectinate scales on posterior-lateral margin of first article. Dactylus sharp, strongly hooked.
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Fig. 9

Pereopods 2 to 6 of a praniza larva (P2–P6) of a Gnathia trimaculata n. sp. (W28387). Scale-bar: 200 μm

Pereon. Almost twice as long as wide, wider than cephalosome (Figs. 7A, 11C). Pereonite 1 fused with cephalosome, visible dorsally (Fig. 10D). Pereonite 2 with anterior constriction separating it medially from pereonite 1. Pereonite 4 twice as wide as long; lateral sides taper towards rounded posterior margin; posterior margin extends over pereonite 5 (Fig. 7A); lateral shields at leg attachment. Pereonite 5 consists of elastic membrane, fully expanded with blood meal in praniza-stage; bulbous shields present on lateral sides at leg attachment. Pereonite 6 rectangular; posterior margin slightly concave; lateral shields at leg attachment. Pereonite 7 visible dorsally, small with rounded posterior margin, overlaps first pleonite. Sensory pits and short simple-like setae randomly distributed over all pereonites.

Pleon. Pleon and pleotelson 1/2 length of pereon. Five pleonites visible dorsally (Fig. 7A). Single simple seta on posterior lateral side of each pleonite.

Pleotelson. Triangular, almost as long as wide; anterior half of lateral margins slightly concave; posterior half straight; 3 pairs of simple setae present on dorsal surface. Distal apex terminates in pair of simple setae; anterior half of dorsal surface covered with pectinate scales (Fig. 7E).

Pleopod. Endopod same length as exopod. Endopod with 8 long pappose setae; exopod with 9 long pappose setae distally (Fig. 7F). Sympodite with retinaculae, single plumose seta on lateral margin and short hair-like setae on dorsal surface and margins. Pleopods 2–5 similar to pleopod 1.
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Fig. 10

Scanning electron micrographs of Gnathia trimaculata n. sp., male (A,B), female (C) and larvae (D). A Ventral view of male frontal border; B View of male mandible; C Dorsal view of female cephalosome; D Dorsal view of larva cephalosome. Scale-bars: A, 50 μm; B, 200 μm; C,D, 100 μm

Pereopods. Basis of pereopod 2 subquadrate, with single simple seta anteriorly and posteriorly (Fig. 9A). Ischium 3/4 length of basis and almost as wide, with single simple seta, 1 plumose seta and 1 tooth-shaped tubercle present anteriorly. Merus 1/2 length of ischium, with anterior bulbous protrusion, single elongate denticulate seta and 2 simple setae on bulbous protrusion; posterior margin with simple setae and 1 plumose seta. Carpus almost same size and shape as merus, but without anterior bulbous, tooth-shaped tubercle and single plumose seta on posterior margin. Propodus about twice length of carpus, with 2 robust serrate setae on distal part of posterior side and single simple seta situated anteriorly. Dactylus 1/2 length of propodus, terminates in sharp posterior-pointing unguis; prominent robust seta on posterior side proximal to unguis; 2–3 simple setae on dorsal and ventral sides of robust seta. Pereopods 3–6 (Fig. 9A) similar to pereopod 2 in basic form, differ in setation. Pereopods 3–5 without elongate denticulate setae; pereopod 6 with 2 elongate serrate setae on bulbous protrusion of merus and 2 on posterior side of propodus.

Uropod. Rami extend beyond apex of pleotelson. Endopod longer and wider than exopod; both with long fringing setae; endopod with 6 medial plumose setae; exopod with 4 distal plumose setae plus single simple and single plumose seta laterally (Fig. 7E). Anterior dorsal areas of exopods covered with pectinate scales; all margins with short hair-like setae. Uropodal basis with single simple seta.

Live specimens. In general, larvae yellow-greenish in colour (Fig. 11D), but with striking yellow, brown and black pigmentation on dorsal surface of pereon (Fig. 11C). Three pairs of distinct black spots within yellow circles present on lateral sides of pereonites 4, 5 and 6 (Fig. 11D). Spots present on pereonites 5 and 6 of equal size, twice as large as those on pereonite 4. Three black lines extend dorsally from anterior margin of pereonite 4 to posterior limit of pereonite 6. Two black stripes present on dorsal area of pereonites 2 and 3; these lines reach onto dorsal surface of cephalosome, where they meet in half moon-shape.
https://static-content.springer.com/image/art%3A10.1007%2Fs11230-008-9158-2/MediaObjects/11230_2008_9158_Fig11_HTML.jpg
Fig. 11

Light micrographs of Gnathia trimaculata n. sp., male (A), female (B) and praniza (C,D). A Dorsal view of male; B Dorsal view of female; C Dorsal view of praniza; D Dorsal and lateral view of praniza. Scale-bars: 1 mm

Remarks

Adult male

Gnathia trimaculata can be identified by having three black stripes dorsally and three pairs of brown spots laterally on the pereon in live specimens, a frontal border with mediofrontal process divided into two lobes which almost touch anteriorly and form a distinct key-hole shape, four to five pairs of long pappose setae present ventrally on both lobes, a mandible with seven to eight processes on the dentate blade, a cluster of setae between all processes and an armed carina.

Specimens of G. trimaculata were collected from the same locality as G. grandilaris (see Coetzee et al., 2008). Both these species have long pappose setae and many tubercles randomly distributed on their pereon and pleon; however G. trimaculata is smaller (4.4 mm) than G. grandilaris (6.8 mm), and their maxillipedal palp article order differs, being 5-7-5-8 for G. trimaculata and 6-8-6-9 for G. grandilaris. The mediofrontal process of the G. trimaculata frontal border is divided into two lobes which almost touch anteriorly and form a distinct key-hole shape, whereas G. grandilaris has an inferior mediofrontal process forming one triangular lobe.

Fifteen gnathiid species are currently known from off Queensland, Australia, and, compared to G. trimaculata, these species have few or no setae on their pereon and pereonites (Holdich & Harrison, 1980). G. asperifrons Holdich & Harrison, 1980 (1.9 mm) has dorsal setae, but is much smaller in size than G. trimaculata (4.4 mm) and has an inferior mediofrontal process. G. biorbis Holdich & Harrison, 1980 (4.88 mm) falls within the same size range as G. trimaculata, but differs in its triangular mediofrontal process with a slight indented apex.

G. pantherina Smit & Basson, 2002 is the only known South African gnathiid species that parasitises elasmobranchs. The males of this species have long pappose setae on their pleon and pleonites and have a similar shaped pleotelson and uropod to G. trimaculata. However, G. pantherina (5.6 mm) is bigger than G. trimaculata (4.4 mm), has a V-shaped frontal border with a deeply divided mediofrontal process, and rows of long plumose setae reaching the median tubercle (Smit & Basson, 2002). Live G. pantherina males have distinctive brown-red markings on the anterior end of the cephalosome, pereon and pleon, reaching from the anterior end of pereonite 2 to the posterior margin of pereonite 6 (Smit & Basson, 2002).

The larvae of Gnathia capillata Nunomura & Honma, 2004 are found parasitising stingrays and gummy sharks from off Sado Island, Sea of Japan. The males of G. capillata (7.6 mm) are bigger than G. trimaculata (4.4 mm), they lack a frontolateral process, and the mediofrontal process is raised and has a slightly indented apex (Nonumura & Honma, 2004).

Adult female

Owing to the lack of comprehensive descriptions of female gnathiids in general, it is difficult to compare the female of G. trimaculata with those of the other Australian species accurately. However, Smit & Basson (2002) included a complete description of G. pantherina females. G. trimaculata and G. pantherina females have a similar shaped cephalosome and pleotelson. Maxillipedal palp setae of G. trimaculata females are in the order 4-6-5-7, while the order for G. pantherina is 8-7-5-10. G. trimaculata females are yellow, with dark half moon-shaped pigmentation on the dorsal cephalosome, three black pigment stripes on the dorsal surface of pereonites 4, 5 and 6, and three pairs of dark spots laterally on the pereon. They also have light brown–red markings on the anterior end of the cephalosome (Smit & Basson, 2002).

Pranizae

Descriptions of Australian gnathiid larvae are usually poor and thus it has been impossible to use them for comprehensive comparisons. G. grandilaris juveniles are not only known from Australian elasmobranchs but have been recorded on the same host (grey reef shark) as G. trimaculata. Despite sharing a common host, the shape of their cephalosome and the few setae found on their pereon, they do demonstrate important morphological differences. G. grandilaris pranizae (6.1 mm) are larger than those of G. trimalculata (4.0 mm); they also differ in pleotelson shape and in the number of marginal setae found on the exopod and endopod of the second pleopod. G. grandilaris pranizae have nine teeth on each mandible, whereas G. trimaculata juveniles have eight. In comparison with G. pantherina, the maxillule of G. trimaculata has six small teeth, while G. pantherina has seven. G. pantherina and G. grandilaris pranizae also have a coupling hook on the maxilliped, which is absent from G. trimaculata. Live G. trimaculata pranizae are yellow-greenish in colour; three black lines extend dorsally from the anterior margin of pereonite 4 to the posterior limit of pereonite 6, and three pairs of distinctive black spots within yellow circles occur on the lateral sides of pereonites 4, 5 and 6. Live G. grandilaris pranizae have a black pereon with white markings, while the dorso-lateral surfaces of the pleon have light brown pigmentation patterns, reaching from the posterior rim of pleonite 1 to the anterior margin of pleonite 5 (Coetzee et al., 2008). The Japanese G. capillata pranizae has also eight teeth on its mandible, as in G. trimaculata, but can easily be distinguished from this species because of its large size (8 mm) and many setae on its body surface.

General discussion

Currently no information exists on the life-cycle of gnathiids parasitising elasmobranchs, but it may follow the three larval stage pattern described for other Gnathia species (Smit et al., 2003). All juveniles collected from the sharks were praniza stages (fed stages); it is interesting to note that they moulted into adults, and thus were third-stage pranizae. This raises the question of where the first- and second-stage pranizae might be found. According to McKiernan et al. (2005), younger juveniles may avoid elasmobranchs due to their thick skin, which makes it too difficult for attachment, and thus they may prefer to feed on teleosts. However, if these younger stages are also attached to the gills and septum of elasmobranchs, this might not apply.

Acknowledgements

Many thanks to the Lizard Island Research Station Staff, Will Robins (James Cook University, School of Marine and Tropical Biology, Townsville) and Tom Lisney (The University of Queensland, School of Biomedical Sciences, Brisbane) for collecting the sharks. This study was funded by an Australian Research Council Discovery Grant and the Sea and Coast II Programme of the National Research Foundation of Southern Africa.

Copyright information

© Springer Science+Business Media B.V. 2008