JOURNAL OF CRUSTACEAN BIOLOGY, 23(2): 341–351, 2003 ZOEAL DEVELOPMENT OF HETEROPILUMNUS CILIATUS (DECAPODA: PILUMNIDAE), WITH A KEY TO THE KNOWN PILUMNID ZOEAS IN KOREA AND ADJACENT WATERS Hyun Sook Ko and Hoi Jeong Yang Department of Life Sciences, Silla University, Busan 617-736, Republic of Korea (corresponding author (HSK) [email protected]) Downloaded from https://academic.oup.com/jcb/article/23/2/341/2679814 by guest on 24 September 2021 ABSTRACT An ovigerous crab of Heteropilumnus ciliatus (Stimpson) was collected in South Korean waters, and the larvae were reared in the laboratory. Three zoeal stages are described and illustrated in detail. Morphological characteristics of the first zoea of H. ciliatus differ from those described by Takeda and Miyake (1968). The first zoea of H. ciliatus appears to be similar to the first zoeas of Heteropanope glabra Stimpson and Pilumnopeus makiana (Rathbun), but they can be distinguished from each other by differences of the carapace spines. A provisional key is provided to aid the identification of the pilumnid zoeas in Korea and adjacent waters. In the family Pilumnidae, the complete larval drawings were made with the aid of camera lucida. Setal development has been described for eleven counts and measurements were based on about 10 specimens for each zoeal stage. The sequence of the zoeal description is species, whereas only the zoeal stages have based on the malacostracan somite plan and described from been described for five species. Ten of the anterior to posterior. Setal armature of appendages is de- sixteen species have been recorded in Korean scribed from proximal to distal segments and in order of and adjacent waters including Japan and China endopod to exopod (see Clark et al., 1998). The zoeal stages (see Table 1). are described and fully illustrated. For the second and third zoeal stages, only the main differences from the previous The pilumnid crab Heteropilumnus ciliatus stage are described. The long, plumose natatory setae of the (Stimpson, 1858) is found under stones or in first and second maxillipeds and the long antennular crevices of rocks in shallow waters (Sakai, aesthetascs were drawn truncated. The zoeal series and the 1976). The species is the only representative of spent female are deposited at Silla University, Korea. the genus found in Korea, and it also occurs on RESULTS the coasts of North China and Japan (Kim, 1973; Sakai, 1976; Dai and Yang, 1991). The Three zoeal stages occurred before meta- first zoea of H. ciliatus was first described by morphosis to the megalop stage. The durations Takeda and Miyake (1968), but that report was of the zoeal stages I–III at 258C were 4, 6, and 5 limited to brief comments and illustrations. The days, respectively. aim of this paper is to describe the zoeal stages Heteropilumnus ciliatus (Stimpson, 1858) of H. ciliatus in detail, to compare its morphology with previously described pilumnid Heteropilumnus ciliatus Takeda and Miyake, 1968: 127, fig. 3–4a–k, zoea I. zoeas, and to provide a key to the known pilummid zoeas in Korea and adjacent waters. Zoea I Figs. 1, 2 MATERIALS AND METHODS Size.—Carapace length 0.61 6 0.06 mm. One ovigerous crab of Heteropilumnus ciliatus was Distance from tip of dorsal spine to tip of collected by Hyun Sook Ko by SCUBA diving from Chuja Island, off the southern part of Korea, 2 July 2001 and rostral spine 1.93 6 0.05 mm. transported to a constant-temperature chamber at Silla University, Busan. The first stage zoeas hatched on 22 Aug Carapace (Fig. 1A, B, C).—Dorsal spine long, 2001 and were reared using methods described by Ko (1995) distally slightly curved and spinulate, longer at a constant water temperature of 258C. Larvae were fixed than rostral spine; rostral spine straight and and preserved in 10% neutral Formalin. Zoeal specimens slightly longer than antennal protopod; lateral were dissected using Leitz zoom stereomicroscope, and appendages were examined under a Leitz Laborlux S spines present and short; anterodorsal setae microscope. Appendages were mounted in polyvinyl lacto- absent; 1 pair of posterodorsal setae present; phenol, cover slips were sealed with clear nail varnish, and ventral margins without setae; eyes sessile. 341 342 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 2, 2003 Table 1. Earlier descriptions of larval development of species in the family Pilumnidae. Recorded in Korea and Species Complete larval development Zoeal stages only adjacent waters Heteropanope glabra Stimpson Lim et al. (1984) Greenwood X and Fielder (1984a) P. lumpinus Bennett Wear (1967) P. novaezealandiae Filhol Wear (1967) Pilumnus dasypodus Kingsley Bookhout and Costlow (1979) P. vespertilio (Fabricius) Lim and Tan (1981) X P. hirtellus (Linnaeus) Salman (1982) P. minutus De Haan Ko (1994b) X Parapilumnus trispinosus Sakai Ko (1994a) X Downloaded from https://academic.oup.com/jcb/article/23/2/341/2679814 by guest on 24 September 2021 B. eucratoides (Stimpson) (as Pilumnopeus eucratoides) Lim et al. (1986) X Benthopanope indica (de Man) Ko (1995) Wear (1968) X P. serratifrons (Kinahan) Greenwood and Fielder (1984b) Pilumnopeus makiana (Rathbun) Lee (1993) X Pilumnopeus granulata Balss Ko (1997) X Heteropilumnus ciliatus (Stimpson) Takeda and Miyake (1968) X Actumnus setifer (De Haan) Aikawa (1937) X Tanaocheles bidentata (Nobili) Ng and Clark (2000) Antennule (Fig. 1D).—Uniramous; endopod Second Maxilliped (Fig. 2B).—Coxa without absent; exopod unsegmented, with 3 long (2 seta; basis with 4 setae; endopod 3-segmented, stout 1 thinner) aesthetascs, 1 short, slender with 1, 1, 6 (3 subterminal 1 3 terminal) setae aesthetasc, and 2 small setae, all terminal. respectively; exopod 2-segmented, distal seg- ment with 4 terminal natatory plumose setae. Antenna (Fig. 1E).—Protopod slightly shorter than rostral spine and distally spinulate; exopod Third Maxilliped.—Present but small. slightly longer than protopod and distally Pereiopods (Fig. 2C).—Developing; cheliped spinulate on both lateral margins, with 1 larger bilobed. and 1 small medial spines. Endopod developing. Abdomen (Fig. 2E).—5 somites; somite 2 with Mandibles (Fig. 1F).—Asymmetrical; right pair of lateral processes directed laterally; molar with 4 teeth, left molar with 1 tooth, somite 3 with pair of lateral processes directed confluent with incisor process; endopod palp posteriorly; somites 2–5 each with 1 pair of absent. posterodorsal setae; pleopods absent. Maxillule (Fig. 1G).—Epipod seta absent, Telson (Fig. 2D, E).—Each fork long and coxal endite with 7 terminal setae; basial endite spinulate, with 1 stout lateral spine, 1 minute with 5 setal processes; endopod 2-segmented, lateral seta and 1 dorsomedial spine; posterior proximal segment with 1 seta, distal segment margin with 3 pairs of stout spinulate setae. with 6 (2 subterminal 1 4 terminal) setae; exopod seta absent. Zoea II Figs. 3, 4 Maxilla (Fig. 1H).—Coxal endite bilobed, with 614 setae; basial endite bilobed, with 514 Size.—Carapace length 0.86 6 0.08 mm. setae; endopod bilobed, with 315(2sub- Distance from tip of dorsal spine to tip of terminal 1 3 terminal) setae; exopod (scaphog- rostral spine 2.18 6 0.08 mm. nathite) margin with 4 plumose setae plus distal Carapace (Fig. 3A, B, C).—2 pairs of ante- stout process. rodorsal setae present; each ventral margin with First Maxilliped (Fig. 2A).—Coxa without 5 plumose setae; eyes stalked; otherwise un- seta; basis with 10 setae arranged 2, 2, 3, 3; changed. endopod 5-segmented, with 3, 2, 1, 2, 5 (1 Antennule (Fig. 3D).—Exopod now with 6 long subterminal 1 4 terminal) setae respectively; (3 stout 1 3 thinner) terminal and 1 subterminal exopod 2-segmented, distal segment with 4 aesthetascs plus 1 terminal seta, otherwise un- terminal natatory plumose setae. changed. KO AND YANG: ZOEAL DEVELOPMENT OF HETEROPILUMNUS CILIATUS 343 Downloaded from https://academic.oup.com/jcb/article/23/2/341/2679814 by guest on 24 September 2021 Fig. 1. Heteropilumnus ciliatus, first zoeal stage. A, lateral view; B, frontal view; C, lateral expansion of carapace; D. antennule; E, antenna; F, mandibles; G, maxillule; H, maxilla. Scale bars, A, B 5 0.5 mm; D, E, G, H 5 0.1 mm; C, F 5 0.25 mm. 344 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 2, 2003 Downloaded from https://academic.oup.com/jcb/article/23/2/341/2679814 by guest on 24 September 2021 Fig. 2. Heteropilumnus ciliatus, first zoeal stage. A, first maxilliped; B, second maxilliped; C, pereiopods; D, fork of telson; E, dorsal view of abdomen and telson. Scale bars, A, B, C, D 5 0.1 mm; E 5 0.5 mm. KO AND YANG: ZOEAL DEVELOPMENT OF HETEROPILUMNUS CILIATUS 345 Downloaded from https://academic.oup.com/jcb/article/23/2/341/2679814 by guest on 24 September 2021 Fig. 3. Heteropilumnus ciliatus, second zoeal stage. A, lateral view; B, frontal view; C, lateral expansion of carapace; D, antennule; E, antenna; F, mandibles; G, maxillule; H, maxilla. Scale bars, A, B, C 5 0.5 mm; F 5 0.25 mm; D, E, G, H 5 0.1 mm. 346 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 2, 2003 Antenna (Fig. 3E).—Endopod more developed; Maxilla (Fig. 5H).—Basial endite bilobed with otherwise unchanged. 616 setae; exopod (scaphognathite) margin with 19 plumose setae; otherwise unchanged. Mandibles (Fig. 3F).—Unchanged. First Maxilliped (Fig. 6A).—Coxa with epipod Maxillule (Fig. 3G).—Epipod seta now present; bud present; endopod terminal segment with 6 basial endite with 8 setal processes; exopod (2 subterminal 1 4 terminal) setae; exopod plumose seta now present; otherwise unchanged. distal segment now with 8 terminal natatory Maxilla (Fig. 3H).—Basial endite bilobed with plumose setae; otherwise unchanged. 615 setae; exopod (scaphognathite) margin Second Maxilliped (Fig. 6B).—Coxa with with 14 plumose setae, distal, stout process no epipod bud present; exopod distal segment Downloaded from https://academic.oup.com/jcb/article/23/2/341/2679814 by guest on 24 September 2021 longer prominent; otherwise unchanged.