The First Zoeal Stages of Parapanope euagora and Halimede fragifer (Decapoda: Pilumnoidea: Galenidae) Hatched in the Laboratory

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  • ABSTRACT

    The first zoeas of Parapanope euagora and Halimede fragifer hatched in the laboratory from two ovigerous galenid crabs of Pilumnoidea were collected from Jindo Island, Jeolanam-do, southern Korea. Their morphologies are described in P. euagora for the first time in the world and re-described in H. fragifer with the color images of live zoeas. In this study, they show a general morphology of Pilumnoidea by having a long antennal exopod, an endopod of the maxillule with 1, 2+4 setae, an endopod of the maxilla with 3+5 setae, and a fork of the telson with two lateral armatures. However, the first zoea of P. euagora differs from other known zoeas of pilumnoid species including H. fragifer by having a long antennal exopod with a medial seta and spine, not two spines, and a fork of telson with two lateral setae, not a seta and spine. Such characteristics of the antennal exopod and the fork of telson are reported for the first time in the pilumnoid zoeas. A comparison between the first zoeal stage of H. fragifer in this study and that of Terada shows minute differences in the characteristics of the antennule and the fork of telson.


  • KEYWORD

    Galenidae , first zoea , Parapanope euagora , Halimede fragifer , Korea

  • Introduction

    The crabs of the Pilumnoidea are recognized by the following characteristics of all male abdominal somites freely articulating, a long and slender gonopod 1, a very short and sigmoidal gonopod 2, and a penis which protrudes from the condyle of the fifth ambulatory coxa (Ng et al., 2008). At present, over 390 species of three families (Galenidae, Pilumnidae, and Tanaochelidae) have been recorded in the world. Over 380 species of the Pilumnidae exist in the world, and 15 species are known from Korean waters (Table 1). In the Galenidae, 12 species are reported in the world (Ng et al., 2008). Among them, only two species, Parapanope euagora De Man 1895 and Halimede fragifer (De Haan 1835) are recorded from Korean waters (Table 1).

    In the Pilumnoidea, larval descriptions of Pilumnidae are known for nine species belonging to six genera from Korea and adjacent waters (Table 1). The larval description of Galenidae is only available for the first and second zoeal stages of H. fragifer described by Terada (1985), however, his description is not adequate for the modern larval description suggested by Clark et al. (1998). The larval stage of P. euagora is unknown until now. Therefore, the aims of this study are to describe and illustrate the first zoeal stages of P. euagora and H. fragifer in detail and compare their morphologies with the previously described zoeas of the Pilumnoidea.

    Materials and Methods

    Ovigerous crabs were collected in the intertidal region in Jindo-gun, Jeolanam-do, southern Korea on 26 Jul 2012 for Parapanope euagora and 26 Jul 2013 for Halimede fragifer. The first zoeas hatched in the laboratory on 28 Jul 2012 for P. euagora and 30 Jul 2013 for H. fragifer, respectively. The first zoeas were preserved in 95% ethyl alcohol for examination. A high mortality followed, and no larvae reached the second zoeal stage. The digital photos of the living zoeas were taken using a Leica EZ40 microscope (Leica, Wetzlar, Germany) and then processed in photoshop. The zoeal specimens were dissected using a Leitz zoom stereomicroscope, and appendages were examined under a Leitz Laborlux S microscope. The appendages were mounted in ethylene glycol and drawings were prepared with the camera lucida. The setal counts on the appendages and the lengths of measurement were based on the mean of 10 specimens of zoeas. The sequence of the zoeal description is based on the malacostracan somite plan and described from the anterior to posterior. The setal armature on appendages is described from the proximal to distal segments and in order of endopod to exopod. The long plumose natatory setae of the first and second maxillipeds were drawn truncated. The chromatophoric patterns were observed with living zoeas. A micrometer was used for the zoeal measurements: carapace length (CL) from the base of the rostral spine to the most posterior carapace margin and rostral and dorsal spine length (RDL) from the tip of the rostral carapace spine to the tip of the dorsal carapace spine. The specimens were examined and the spent females were deposited in Silla University, Korea.

    Results

      >  Parapanope euagora De Man, 1895 (Fig. 1A)

    First zoea (Fig. 1B, 2)

    Size: CL 0.36±0.05 mm; RDL 0.77±0.05 mm.

    Chromatophores (Fig. 1B): black chromatophores which occurring behind eyes and on abdominal somites 1-4 ventrally.

    Carapace (Figs. 1B, 2A, A′): dorsal spine with few minute tubercles, less than CL, slightly longer than rostral spine; rostral spine slightly longer than antennal protopod; lateral spines present, half length of rostral spine; 1 pair of posterodorsal setae present; each ventral margin with spinules; eyes sessile.

    Antennule (Fig. 2B): uniramous; endopod absent; exopod with 2 long, stout aesthetascs, 1 shorter, thinner aesthetasc, 3 unequal simple setae, all terminal.

    Antenna (Fig. 2C): biramous; endopod bud absent; protopod with 2 rows of spinules on distal half; exopod spinulate on distal half, with 2 equal setae medially, tip reaching tip of protopod.

    Mandibles (Fig. 2D): asymmetrical; right molar with 4 teeth, left molar with 3 teeth, confluent with incisor process; palp absent.

    Maxillule (Fig. 2E): coxal endite with 7 setae; basial endite with 5 setae and 2 teeth; endopod 2-segmented, proximal segment with 1 seta, distal segment with 6 (2 subterminal, 4  terminal) setae; exopod seta and epipod absent.

    Maxilla (Fig. 2F): coxal endite bilobed, with 6+4 setae; basial endite bilobed, with 5+4 setae, 1 tooth; endopod bilobed, with 3+5 setae; exopod (scaphognathite) margin with 4 plumose setae, 1 distal process.

    First maxilliped (Fig. 2G): coxa without seta; basis with 10 setae, arranged 2+2+3+3; endopod 5-segmented, with 3, 2, 1, 2, 5 (1 subterminal, 4 terminal) setae; exopod 2-segmented, distal segment with 4 long terminal plumose natatory setae.

    Second maxilliped (Fig. 2H): coxa without seta; basis with 4 setae, arranged 1+1+1+1; endopod 3-segmented, with 1, 1, 6 (2 subterminal, 4 terminal) setae; exopod 2-segmented, distal segment with 4 long terminal plumose natatory setae.

    Abdomen (Fig. 2I): five somites; somite 2 with 1 pair of lateral processes directed anteriorly; somite 3 with 1 pair of lateral processes directed posteriorly; somites 2-5 each with 1 pair of posterodorsal setae; pleopod absent.

    Telson (Fig. 2I, I′): each fork extremely long, spinulated laterally, with 2 lateral setae, 1 dorsomedial spine; posterior margin with 3 pairs of setae.

      >  Halimede fragifer (De Haan 1835) (Fig. 1C)

    First zoea (Figs. 1D, 3)

    Size: CL 0.42±0.03 mm; RDL 0.92±0.02 mm.

    Chromatophores (Fig. 1D): yellowish brown chromatophores which occurring behind eyes, on basis of dorsal spine posteriorly, on basis of each maxilliped, on abdominal somites 1, 2 medially, margins of abdominal somites 4, 5 posteriorly, telson ventrally.

    Carapace (Figs. 1D, 3A, A′): dorsal spine with few minute tubercles, slightly less than CL, twice longer than rostral spine; rostral spine slightly shorter than antennal protopod; lateral spines present, half length of rostral spine; 1 pair of posterodorsal setae present; each ventral margin with spinules; eyes sessile.

    Antennule (Fig. 3B): uniramous; endopod absent; exopod with 2 long, stout aesthetascs, 2 shorter, thinner aesthetascs, 2 unequal simple setae, all terminal.

    Antenna (Fig. 3C): biramous; endopod bud absent; protopod with 2 rows of spinules on distal half; exopod spinulate on distal half, with 2 unequal spines medially, tip reaching tip of protopod.

    Mandibles (Fig. 3D): asymmetrical; right molar with 3 teeth, left molar with 4 teeth, confluent with incisor process; palp absent.

    Maxillule (Fig. 3E): coxal endite with 7 setae; basial endite with 5 setae and 3 teeth; endopod 2-segmented, proximal segment with 1 seta, distal segment with 6 (2 subterminal, 4 terminal) setae; exopod seta and epipod absent.

    Maxilla (Fig. 3F): coxal endite bilobed, with 6+4 setae; basial endite bilobed, with 5+4 setae, 1 tooth; endopod bilobed, with 3+5 setae; exopod (scaphognathite) margin with 4 plumose setae, 1 distal process.

    First maxilliped (Fig. 3G): coxa without seta; basis with 10 setae, arranged 2+2+3+3; endopod 5-segmented, with 3, 2, 1, 2, 5 (1 subterminal, 4 terminal) setae; exopod 2-segmented, distal segment with 4 long terminal plumose natatory setae.

    Second maxilliped (Fig. 3H): coxa without seta; basis with 4 setae, arranged 1+1+1+1; endopod 3-segmented, with 1, 1, 6 (3 subterminal, 3 terminal) setae; exopod 2-segmented, distal segment with 4 long terminal plumose natatory setae.

    Abdomen (Fig. 3I): five somites; somite 2 with 1 pair of lateral processes directed laterally; somites 3-5 each with 1 pair of lateral processes directed posteriorly; somites 2-5 each with 1 pair of posterodorsal setae and 8 denticles on posterior margin; pleopod absent.

    Telson (Fig. 3I): each fork long, covered with spinules, with 1 stout lateral spine, 1 minute lateral seta and 1 stout dorsomedial spine; posterior margin with 3 pairs of setae.

    Discussion

    The first zoeal stage of Parapanope euagora is described for the first time, and the first zoeal stage of Halimede fragifer is redescribed in this study.

    Terada (1985) described the first and second zoeal stages of H. fragifer. Hence, the first zoeal characteristics of this study are compared to his description. As a result, minute differences in zoeal size, numbers of antennular aesthetascs, and the spinulate fork of telson (Table 2) were observed. Such differences may be due to preservation techniques of zoeas and overlooking the antennule and fork of telson.

    The first zoeal stage of P. euagora is reported for the first time in this study; therefore, the zoeal description of Galenidae is now available for two species, P. euagora and H. fragifer. It is similar to that of H. fragifer, however, can be distinguished by the following characteristics: The antennule with three aesthetacs and three setae, and the antennal exopod with one seta and one spine medially, the second and third abdominal somites with lateral processes, and the fork of telson with two lateral seate (Table 2).

    Ko and Lee (2012) summarized the morphological characteristics of the first zoeas of Pilumnoidea as follows: long antennal exopod and protopod wih subequal length, and the antennal exopod with two medial spines; the endopods of the maxillule and maxilla each have 1, 2+4 setae, and 3+5 setae, respectively; and the fork of telson has one seta and one spine laterally. The first zoeal stage of H. fragifer agrees well with the known zoeas of Pilumnoidea, but that of P. euagora differs from them by having the antennal exopod with one seta and one spine medially and the fork of telson with two setae laterally (Table 3). Such types of the antennal exopod and the fork of telson are reported for the first time in the Pilumnoidea, therefore, a re-evaluation of the taxonomic status of P. euagora should be needed.

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  • [Table 1.] List of species of the superfamily Pilumnoidea from Korean waters and its known larval stages
    List of species of the superfamily Pilumnoidea from Korean waters and its known larval stages
  • [Fig. 1.] Color photos of crab and the first zoeas of Parapanope euagora and Halimede fragifer. A, Crab of P. euagora; B, First zoeas of P. euagora; C, Crab of H. fragifer; D, First zoeas of H. fragifer.
    Color photos of crab and the first zoeas of Parapanope euagora and Halimede fragifer. A, Crab of P. euagora; B, First zoeas of P. euagora; C, Crab of H. fragifer; D, First zoeas of H. fragifer.
  • [Fig. 2.] Parapanope euagora, first zoeal stage. A, Lateral view; A', Lateral expansion of carapace; B, Antennule; C, Antenna; D, Mandibles; E, Maxillule; F, Maxilla; G, First maxilliped; H, Second maxilliped; I, Dorsal view of abdomen and telson; I', Fork of telson. Scale bars: A=0.3 mm, I=0.2 mm, A', B-H, I'=0.1 mm.
    Parapanope euagora, first zoeal stage. A, Lateral view; A', Lateral expansion of carapace; B, Antennule; C, Antenna; D, Mandibles; E, Maxillule; F, Maxilla; G, First maxilliped; H, Second maxilliped; I, Dorsal view of abdomen and telson; I', Fork of telson. Scale bars: A=0.3 mm, I=0.2 mm, A', B-H, I'=0.1 mm.
  • [Fig. 3.] Halimede fragifer, first zoeal stage. A, Lateral view; A', Lateral expansion of carapace; B, Antennule; C, Antenna; D, Mandibles; E, Maxillule; F, Maxilla; G, First maxilliped; H, Second maxilliped; I, Dorsal view of abdomen and telson. Scale bars: A=0.3 mm, I=0.2 mm, A', B-H=0.1 mm.
    Halimede fragifer, first zoeal stage. A, Lateral view; A', Lateral expansion of carapace; B, Antennule; C, Antenna; D, Mandibles; E, Maxillule; F, Maxilla; G, First maxilliped; H, Second maxilliped; I, Dorsal view of abdomen and telson. Scale bars: A=0.3 mm, I=0.2 mm, A', B-H=0.1 mm.
  • [Table 2.] Comparison of the first zoeal characteristics between Halimede fragifer and Parapanope euagora of the family Galenidae
    Comparison of the first zoeal characteristics between Halimede fragifer and Parapanope euagora of the family Galenidae
  • [Table 3.] Comparison of the first zoeal characteristics for the Pilumnoidea from Korean waters
    Comparison of the first zoeal characteristics for the Pilumnoidea from Korean waters