Caligus undulatus Shen and Li, 1959

Moon, Seong Yong & Park, Jong Sick, 2019, Occurrence of sea lice, Caligus undulatus Shen and Li, 1959 (Copepoda: Siphonostomatoida: Caligidae) in plankton samples collected from Korea, Journal of Species Research 8 (4), pp. 365-372 : 366-371

Caligus undulatus Shen and Li, 1959

Korean name: Tteo-dol-i-mul-i ḓūjḏj (flḋ) ( Figs. 2-4 )

Caligus undulatus Shen and Li, 1959: 12 , 16, pl. 1; Yamaguti, 1963: p. 61, pl. 80, fig. 3; Pillai, 1966: 123, fig. 1; Margolis et al., 1975: p. 81; Montú, 1982: 329; Venmathi Maran and Ohtsuka, 2008: 206, figs. 3I- O, 4A- M; Suárez-Morales et al., 2012b: 805, figs. 1, 2; Venmathi Maran et al., 2012b: 212 , fig. 8D, E.

Material examined. One female (left antenna dissected on glass slide, 1 vial) (NIBRIV0000282332), Gangjin Bay (34°49 ʹ 31 ʺ N, 127°47 ʹ 23 ʺ E), Jeollanam-do Province, southern Korea, 12 September, 2012, Jong Sick Park ; four females and three males, the Mokpo Harbour (34°49 ʹ 31 ʺ N, 127°47 ʹ 23 ʺ E) (NIBRIV0000293068), Jeollanam-do Province, western Korea, 2 August, 2013, Seong Yong Moon .

Description. Female. Body ( Fig. 2A ) 3.08-4.46 mm (mean 3.52± 0.54 mm) in length excluding caudal setae. Cephalothoracic shield slightly ovoid, 1.38 times longer than width (2.16 × 1.56 mm); lateral zone with smoothly curved ventral rib; posterior sinus deep; posterolateral pit present. Fourth pedigerous somite indistinctly articulated from genital complex. Genital complex ( Fig. 2A ) with trapezoidal-shaped and/or a peculiar irregular undulation, gradually broadened distally, 1.17 × 1.11 mm, with rounded and slightly projected posterolateral corners. Abdomen ( Figs. 2A , 3A ) indistinctly separated from genital complex and 2-segmented; first segment wider than length (0.22 × 0.35 mm); distal segment 1.75 times longer than width (0.56 × 0.32 mm). Caudal ramus ( Fig. 2B ) 1.92 times longer than width (0.23 × 0.12 mm), with 6 plumose setae (seta I lacking); inner margin convex, with setules on distal half. Antennule ( Fig. 2C ) 411 μm long and 2-segmented; proximal segment 73% length of antennule, with 25 pinnate and 2 naked setae; distal segment with 12 naked setae and 2 aesthetascs. Antenna ( Fig. 2D ) 3-segmented; proximal segment with proximal process; second segment nearly quadrangular, with 1 adhesion pad on ventromedial margin; distal segment forming long, distally strongly bent claw bearing 2 small setae. Post-antennal process ( Fig. 2E ) long and narrow, proximally bearing 2 papillae, each tipped with 2 setules; another papilla locat- ed posterior to post-antennal process also tipped with 2 setules. Mandible ( Fig. 2F ) with 12 teeth distally. Maxillule ( Fig. 2G ) consisting of anterior papilla bearing 3 unequal setae and tapering posterior process. Maxilla ( Fig. 2H, I ) 2-segmented; proximal segment (lacertus) large and unarmed; slender distal segment (brachium) with membrane (flabellum) at about 60% region of inner margin; calamus about twice as long as canna. Maxilliped ( Fig. 2J ) 3-segmented; proximal segment (corpus) with broader proximal half and narrower distal half; second segment (shaft) 1 seta distally; distal segment forming long, curved claw. Sternal furca ( Fig. 2K ) with slender, long tines bearing membrane on lateral sides. Armature formula of legs 1-4 as follows (Roman numerals: number of spines; Arabic numerals: number of setae):

Leg 1 ( Fig. 3B, C ) intercoxal sclerite naked and elongate. Coxa with simple outer seta. Basis with pinnate outer and inner setae. Exopod 2-segmented; first segment with 1 small outer distal naked seta and row of setules on inner margin; second segment with 3 apical spines, middle and inner apical spines with accessory process, inner distal seta naked and shorter than mid-terminal setae; endopod small, knob-like.

Leg 2 ( Fig. 3D ) intercoxal sclerite subquadrate, with hyaline membrane along distal margin. Coxa with large seta on inner posterior margin and one setule on anterior surface. Basis with small outer seta and one inner setule and membrane on inner part of posterior margin; outer side of basis and first exopodal segment with broad membrane. Exopod 3-segmented, with large hyaline membrane covering dorsal surface of ramus; first segment with 1 inner plumose seta, row of setules along inner margin and pectinate membrane at base of outer serrate spine; second segment with 1 inner plumose seta, short row of setules along proximomedial margin, 1 outer serrate spine on anterior surface; distal segment with 5 inner plumose setae, one serrated spine, and 2 outer small spines on mediolateral margin. Endopod 3-segmented; first segment with 1 long inner plumose seta, row of setules along most of outer margin; second segment with 2 inner plumose setae and row of large setules along most of outer margin; distal segment with spinules at base of 6 plumose setae and row of setules along proximolateral and proximomedial margins.

Leg 3 ( Fig. 3E ) protopod broad membrane on outer and inner margins and with 1 outer naked and 1 inner plumose seta, velum between rami, corrugated patched on dorsolateral surface, 2 marginal membranes, 2 long setules along posterior margin; exopod 3-segmented; first segment ( Fig. 3F ) with 1 outer long setule and spinulate spine, with hyaline membrane at base; second segment with 1 inner plumose seta and 1 outer seta; distal segment with 4 plumose setae, 3 naked spines, setules along the outer margin. Endopod 2-segmented; first segment with 1 inner long plumose seta; second segment with 6 plumose setae and setules along outer margin.

Leg 4 ( Fig. 3G, H ) uniramous, composed of protopod and 2-segment exopod; protopod with 1 distolateral pinnate seta; first exopodal segment with pectinate membrane at base of outer spinulate spine; second exopodal segment with 3 unequal apical spinulate spines and pectinate membrane at base of innermost spine.

Leg 5 ( Fig. 3I ) represented by 1 seta on knob and 1 seta on papilla at posterolateral margin of genital complex.

Male. Body ( Fig. 4A ) 2.91-4.61 mm (mean 3.72±0.65) in length (excluding caudal setae). Cephalothoracic shield 1.48 times longer than width (2.68 × 1.81 mm). Free fourth pedigerous somite wider than length (516 × 258 μm). Genital complex trapezoidal, slightly longer than width (623 × 561 μm). Abdomen ( Fig. 4B ) 2-segmented; proximal segment slightly longer than width (397 × 382 μm); distal segment 1.65 times longer than width (467 × 283 μm). Caudal ramus ( Fig. 4B ) 2.91 times longer than width (308 × 106 μm), armed as in female. Antennule as in female. Antenna ( Fig. 4C ) 3-segmented, comprising coxa, basis, and 1-segmented endopod incorporating distal claw as in female; proximal segment (coxa) with two weak adhesion pads; second segment (basis) with two adhesion pads; distal segment (endopod) blunt, with two inner proximal setae, distally forming bifurcated structure, and round processes. Post-antennal process ( Fig. 4D ) long and more acutely pointed at tip than female. Mandible and maxilla as in female. Maxillule ( Fig. 4E ) with corrugate surface and one stout hyaline structure on dentiform process. Pair of post oral pads ( Fig. 4F ) present just below oral cone. Maxilliped ( Fig. 4G ) as in female, except proximal segment (corpus) with well protruded quadrilateral knob at midlength; distal segment (claw) long, acutely pointed, with one minute seta on distal half and one long setae located posteriorly along 2/3 of claw. Tines of sternal furca ( Fig. 4H ) noticeably longer than female. Legs 1-4 as in female. Leg 5 ( Fig. 4I ) vestigial, situated mid-laterally on genital complex and bearing two pinnate setae. Leg 6 ( Fig. 4I ) forming genital operculum, with two unequal minute setae on distolateral corner.

Host. Unknown.

Distribution. Korea (Seomjin River Estuary, Gwangyang Bay, Gangjin Bay and Mokpo Harbour); China (Tsingtao Harbour); Japan (off Ube city, the Ariake Sea, Takamatsu Port); India (Palk Bay); Brazil (south Brazilian coast); Mexico (Laguna Chelem, Yucatan). All previous reports on C. undulatus were based on specimens from plankton samples.

Remarks. The original illustration of sea lice C. undulatus by Shen and Li (1959) showed a peculiar irregular undulation of genital complex in female ( Shen and Li, 1959: fig. 1). However, our specimen was trapezoidal-shaped and/or a peculiar irregular undulation of genital complex in female which gradually broadened distally. The shape of genital complex might have been variable during breeding season because all other reports agree with our illustrations (see Pillai, 1966; Venmathi Maran and Ohtsuka, 2008; Suárez-Morales et al., 2012b; Venmathi Maran et al., 2012b).

Body sizes of female specimens in the present study ranged from 3.08-4.46 mm, similar to previous reports ( Shen and Li, 1959; Venmathi Maran and Ohtsuka, 2008). Males in the present study were a little smaller and/or much larger (ranged 2.91-4.61 mm) than those reported from China (3.08 mm in Shen and Li, 1959), India (3.50 mm in Pillai, 1966), Japan and Korea (3.50-3.52 mm in Venmathi Maran and Ohtsuka 2008), and Mexico (2.82 mm in Suárez-Morales et al., 2012b). Nevertheless, our specimens shared characters of C. undulatus , including proportional length of the cephalothoracic shield, genital complex, abdomen, postantennal process, sternal furca, and maxilliped with well protruded quadrilateral knob at midlength in male. We consider that specimens from Korea are C. undulatus with some variation in body size. These facts allow both specimens collected from three different times to be conspecific to each other. They are identified as C. undulatus . Small and large males (2.91- 4.05 mm) of C. undulatus co-occurred in the Mokpo Harbor, southwestern coats of Korea.

The latitudinal distribution of C. undulatus is shown in Fig. 5 . The species was originally recorded from Tsingtao Harbor, China (40°N) by Shen and Li (1959). Our record extends the known latitudinal distribution of C. undulatus southward into the tropical zone of South India (10°N) ( Pillai, 1966) from the Northwest Pacific between 32 to 35°N ( Venmathi Maran and Ohtsuka, 2008; Venmathi Maran et al., 2012b), the previous northern bor- der of its known distributional range. It also represents a modest southwards range extending from the two localities that it was recorded, Mexico (21°N) and Brazil (30°S) in the Atlantic Ocean ( Montú, 1982; Suárez-Morales et al., 2012b), although it has not been reported as a parasite yet. One of the first recorded C. undulatus in the Northwestern Tropical Atlantic and in Mexican waters was reported by Suárez-Morales et al. (2012b). How this species has reached the Americas remains unclear. However, it was probably introduced by aquaculture activities as other Asian fish parasites ( Suárez-Morales et al., 2010). This species has been reported from various countries. Its host might be a highly migratory fish ( Ho and Lin, 2004b; Venmathi Maran and Ohtsuka, 2008). Adults of pelagic caligids have been observed in four genera [ Caligus Müller, 1785 , Lepeophtheirus Nordmann, 1832 , Metacaligus Thomsen, 1949 ( Caligidae ), and Pandarus Leach, 1816 ( Pandaridae Milne Edwards, 1840 )] ( Suárez-Morales et al., 1998; Ho and Lin, 2004b; Venmathi Maran and Ohtsuka, 2008; Venmathi Maran et al., 2012a; Suárez-Morales et al., 2012a; 2012b). Since it is the second record from Korean waters, a detailed parasitological survey of its fish hosts in Korea is necessary to understand host(s) of this particular caligid.

Figures

Fig. 2. Caligus undulatus, adult female from Gangjin Bay, Korea.A. habitus dorsal. B. caudal ramus, dorsal. C. antennules. D. antenna. E. postantennal process. F. mandible.G. maxillule. H. maxilla.I. tip of maxilla. J. maxilliped. K. sternal furca. Scale bars:A =400 μm; B=200 μm; C, H, J, K=100μm; D-G, I=50 μm.

Fig. 3. Caligus undulatus, adult female from Gangjin Bay, Korea.A. genital complex and abodomen, ventral. B. leg 1. C. tip of second exopodal segment of leg 1. D. leg 2. E. leg 3. F. first exopodal segment of leg 3. G, H. leg 4. I. leg 5. Scale bars:A=200μm; B-E, G=100μm; F, H, I=50μm.

Fig. 4. Caligus undulatus, adult male from Mokpo Harbour, Korea.A. habitus, dorsal. B. urosome, dorsal. C. antenna.D. postantennal process. E. maxillule. F. post oral pad. G. maxilliped. H. sternal furca. I. genital segment and legs 5 and 6, ventral. Scale bars: A=400 μm; B, I=200 μm; C-H=100μm.

Fig. 5. Schematic illustration of latitudinal distributions of Caligus undulatus.