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Larval development of the hermit crab Pagurusgracilipes (Stimpson, 1858) (Decapoda: Anomura:Paguridae) reared in the laboratoryELENA S. KORNIENKO a & OLGA M. KORN aa Institute of Marine Biology, Far East Division, Russian Academy of Sciences , 17Pal'chevskogo Str., Vladivostok, 690041, Russia Phone: +7 (4232) 310905 Fax: +7 (4232)310905 E-mail:Published online: 01 Dec 2010.

To cite this article: ELENA S. KORNIENKO & OLGA M. KORN (2007) Larval development of the hermit crab Pagurusgracilipes (Stimpson, 1858) (Decapoda: Anomura: Paguridae) reared in the laboratory, Invertebrate Reproduction &Development, 50:1, 31-46, DOI: 10.1080/07924259.2007.9652224

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Invertebrate Reproduction and Development, 50:1 (2007) 31–46 31Balaban, Philadelphia/Rehovot0168-8170/07/$05.00 © 2007 Balaban

Larval development of the hermit crab Pagurus gracilipes(Stimpson, 1858) (Decapoda: Anomura: Paguridae)

reared in the laboratory

ELENA S. KORNIENKO and OLGA M. KORN*

Institute of Marine Biology, Far East Division, Russian Academy of Sciences,17 Pal’chevskogo Str., Vladivostok 690041, Russia

Tel. +7 (4232) 310905; Fax: +7 (4232) 310900; email: okorn@mail.primorye.ru

Received 11 October 2006; Accepted 8 February 2007

Summary

Larval development of the hermit crab, Pagurus gracilipes (Stimpson, 1858) (Decapoda: Anomura:Paguridae), is described and illustrated from larvae reared in the laboratory. Development includedfour zoea and a single megalopa, thus following the typical pattern in the Paguridae. At atemperature of 22EC larval development took from 19 to 25 days. The main zoeal features allowassignment of P. gracilipes, as well as P. kulkarnii, to Group C of Pagurus larvae (typicalrepresentative: Pagurus anachoretus). Although P. gracilipes, P. hartae, and P. constans wereearlier assigned to the genus Parapagurodes on the basis of adult characters, their larvae representa heterogeneous group and should evidently be placed to different subdivisions of Pagurus larvae.

Key words: Decapoda, hermit crab, Pagurus gracilipes, larval development

Introduction

The hermit crab, Pagurus gracilipes (Stimpson,1858), is known from northern Japan includingHokkaido and northeastern Honshu southward toChoshi, Chiba, as well as from the continental coast ofthe Russian Far East, subtidal to 42 m (Komai, 1998).The taxonomic position of this species is the subject ofdebate. In 1973, McLaughlin and Haig (1973) estab-lished a new genus of hermit crabs, Parapagurodes,with two new species, P. makarovi and P. laurentae. In1996, another new species, Parapagurodes hartae, wasassigned to this genus, with the description of its firstzoeal stage (McLaughlin and Jensen, 1996). In 1998,four species, Pagurus gracilipes, P. nipponensis

(Yokoya, 1933), P. imaii (Yokoya, 1939), and P.constans (Stimpson, 1858), were reexamined and, on thebasis of morphology of sexual tubes in males, trans-ferred from Pagurus to Parapagurodes McLaughlin andHaig, 1973 (Komai, 1998, 1999). However, four speciestransferred from Pagurus to Parapagurodes, includingP. gracilipes, were recently returned to Pagurus(McLaughlin and Asakura, 2004).

Since the morphological features of the larvae ofP. gracilipes are unknown, the aim of this study is thedescription of the complete larval development ofP. gracilipes from laboratory reared material. It is likelythat the information gained will provide an insight intothe taxonomic position of this species.

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Materials and Methods

Ovigerous females of P. gracilipes were collectedfrom Vostok Bay (Peter the Great Bay, Sea of Japan) on11 July 2005 at a depth of 4 m, at 15EC. They weremaintained in an aquarium with aerated seawater untilhatching occurred on 19 July. The crabs were fed withmolluscs every second day and the seawater waschanged daily. After hatching, larvae were concentratedat the edge of aquarium using a point-light source andtransferred to 1 l glass vessels with filtered and UV-sterilized seawater and reared at a temperature of 22EC.The density of the larvae was about 100 specimens perlitre. The larvae were fed newly hatched nauplii ofArtemia salina. The water in the vessels was changeddaily.

The larvae of each stage were fixed in 4%formaldehyde for light microscopy. The chromatophorepattern was determined by observing live larvae. Thefixed larvae were dissected under a MBS-10 stereo-microscope using fine entomological needles. Theoutlines of the larvae and their appendages at thedifferent developmental stages were drawn using acamera lucida attached to a binocular Ergavalmicroscope (Carl Zeiss Jena). Measurements were madewith an ocular micrometer. Methods of measurements,descriptions of setal arrangements and terminologyfollowed that of Clark et al. (1998) and Konishi andShikatani (1998). The carapace length (CL) of zoea andmegalopa was measured from the tip of rostrum to theposterior midpoint of the carapace. The numbering ofthe telsonal posterior setae followed that of Pike andWilliamson (1960). The setal arrangements are listedfrom endopod to exopod, from proximal to distalsegments, and from anterior to posterior abdominalsomites.

Specimens of all larval stages and the spent femalehave been deposited in the Museum of the Institute ofMarine Biology, Russian Academy of Sciences, Vladi-vostok (16201).

Results

P. gracilipes hatched as a prezoeal stage, a fewminutes before moulting to the first zoeal stage. Thetotal time required for larvae to reach the megalopalstage was 19–25 days at 22EC. The body outlines andappendages are illustrated in Fig. 1–7. The diagnosticcharacteristics of each larval stage can be summarized asfollows.

Zoea IDuration. 4–5 days.Size. CL= 1.31 ± 0.03 mm (1.28–1.36 mm, N = 11).

Carapace (Fig. 1A, B). Rostrum tapered, long, about1/3 of carapace length and somewhat longer thanantennal scaphocerite; carapace with low keel anteriorlyin dorsal midline; posterolateral spines short; eyessessile.

Antennule (Fig. 1C). Uniramous, endopod absent;exopod unsegmented, with three terminal aesthetascs(2 long and 1 short), 3 simple terminal setae and a longsubterminal plumose seta.

Antenna (Fig. 1D). Biramous; protopod with strongserrate spine at the base of endopodal junction; endopodfused with protopod, with 2 long terminal plumosesetae; scaphocerite curved, with strong distal spine;outer margin unarmed, inner margin with 9 longplumose setae and a short simple seta.

Mandible (Fig. 1E). Asymmetrically dentate; incisorprocess with a single strong tooth and few small teeth;molar process with serrate ridges and small acuiteddenticles; no palp bud.

Maxillule (Fig. 1F). Endopod 3-segmented, with 1,1, 3 setae; coxal endite with 5 marginal plumo-denticulate setae plus 2 submarginal short simple setae;basial endite with 2 marginal elongate cuspidate setaearmed with few small denticles plus 2 submarginalsimple setae.

Maxilla (Fig. 1G). Endopod bilobed, with 3 plumo-denticulate setae in proximal plus 4 setae in distal lobes;coxal endite bilobed, with 6 marginal + 1 submarginalplumodenticulate setae on proximal lobe and with3 marginal +1 submarginal setae on distal lobe; basialendite bilobed, with 4 marginal + 1 submarginal plu-mose setae on proximal lobe and 3 marginal + 1 sub-marginal plumodenticulate setae on distal lobe;scaphognathite with 5 marginal plumose setae; proximalpart of scaphognathite fused with protopod.

Maxilliped I (Fig. 1H). Endopod 5-segmented, setalformula 3, 2, 1, 2, 4+I (roman number denoting plumosedorsolateral seta) plus numerous microtrichiae on dorsalmargins of segments 1–3; coxa without setae; basis withsetal formula 2, 2, 3, 3; exopod incompletely 2-segmented, with 4 terminal natatory plumose setae.

Maxilliped II (Fig. 1I). Endopod 4-segmented, setalformula 2, 2, 2, 4+I plus numerous microtrichiae ondorsal margins of segments 2–3; coxa without setae;basis with setal formula 1, 2; exopod incompletely 2-segmented, with 4 terminal natatory plumose setae.

Maxilliped III (Fig. 1J). Uniramous, unarmed.Pereopods. Visible as small buds.Abdomen (Fig. 1K). Consists of five somites.

Somites II–V with a pair of lateral and two pairs ofposterodorsal processes, increasing in size posteriorly;somites I–V with two small simple posterodorsal setae.

Telson (Fig. 1K). Fan-shaped posteriorly; the lengthis about equal the width; posterior margin with median

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Fig. 1. Pagurus gracilipes, zoea I. A, lateral view; B, dorsal view; C, antennule; D, antenna; E, mandibles; F, maxillule;G, maxilla; H, maxilliped I; I, maxilliped II; J, maxilliped III; K, dorsal view of abdomen.

cleft and with 7+7 setae: first (outermost) – a shortsmooth spine, second – a fine seta, third through seventh– plumodenticulate articulated setae; a small anal spinepresent on ventral surface.

Uropod absent.

Zoea IIDuration. 4–5 days.Size. CL=1.73 ± 0.07 mm (1.61 – 1.86 mm, N = 12).Carapace (Fig. 2A, B). Eyes stalked; otherwise

unchanged.Antennule (Fig. 2 C). Biramous, endopod as a bud

with a long plumose seta; 2–3 small fine setae on theopposite side; exopod unsegmented, with two terminalaesthetascs (1 long and 1 short) and 4 simple terminalsetae.

Antenna (Fig. 2D). Protopod with strong serratespine and a second small smooth spine at the base ofendopodal junction; endopod unarmed, about 2/3 of

scaphocerite length; scaphocerite length opposite theirwidth about 1/6, outer margin unarmed, inner marginwith 10 long plumose setae.

Mandible (Fig. 2E). Increased in number of smalldenticles; otherwise unchanged.

Maxillule (Fig. 2F). Basial endite with 4 marginalelongate cuspidate setae armed with few small denticlesplus 2 submarginal simple setae; otherwise unchanged.

Maxilla (Fig. 2G). Scaphognathite with 7 marginalplumose setae; otherwise unchanged.

Maxilliped I (Fig. 2H). Endopod with setal formula3+I, 2+I, 1+I, 2, 4+I; exopod with 7 terminal natatoryplumose setae; otherwise unchanged.

Maxilliped II (Fig. 2I). Endopod with setal formula2, 2+I, 2+I, 4+I; exopod with 7 terminal natatoryplumose setae; otherwise unchanged.

Maxilliped III (Fig. 2J). Endopod with 1 terminalsimple setae; coxa and basis unarmed; exopodunsegmented, with 6 terminal natatory plumose setae.

Pereopods. Visible as buds increased in size.

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Fig. 2. Pagurus gracilipes, zoea II. A, lateral view; B, dorsal view; C, antennule; D, antenna; E, mandibles; F, maxillule;G, maxilla; H, maxilliped I; I, maxilliped II; J, maxilliped III; K, dorsal view of abdomen.

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Fig. 3. Pagurus gracilipes, zoea III. A, lateral view; B, dorsal view; C, antennule; D, antenna; E, mandibles; F, maxillule;G, maxilla; H, maxilliped I; I, maxilliped II; J, maxilliped III; K, dorsal view of abdomen.

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Abdomen (Fig. 2K). First and second somites with-out posterodorsal processes; posterodorsal setae arefound only third through fifth somites; otherwiseunchanged.

Telson (Fig. 2K). Increased in length; median cleftabsent; posterior margin with 8+8 setae; anal spine onventral surface poorly visible.

Uropod. Absent.

Zoea IIIDuration. 5–7 days.Size. CL= 2.35 ± 0.06 mm (2.27 – 2.50 mm, N = 11).Carapace (Fig. 3A, B). Unchanged from stage II.Antennule (Fig. 3C). Biramous; protopod with 2

plumose setae at the base of endopod and 3 small simplesetae on the opposite side; endopod as a bud with aplumose terminal seta; exopod with 3 long terminal, 2short subterminal aesthetascs and 3 simple terminalsetae.

Antenna (Fig. 3D). Endopod length about equalscaphocerite length, with small simple seta in distal part;scaphocerite length opposite their width about 8/1;otherwise unchanged.

Mandible (Fig. 3E). Increased in size; otherwiseunchanged.

Maxillule (Fig. 3F). Increased in size; otherwiseunchanged.

Maxilla (Fig. 3G). Scaphognathite with 12 marginalplumose setae; otherwise unchanged.

Maxilliped I (Fig. 3H). Exopod with 7 terminalplumose natatory setae; otherwise unchanged.

Maxilliped II (Fig. 3I). Exopod with 8 terminalplumose natatory setae; otherwise unchanged.

Maxilliped III (Fig. 3J). Exopod incompletely 2-segmented, with 7 (rarely 8) terminal plumose natatorysetae; otherwise unchanged.

Pereopods. Increased in size; pereopod I chelated.Abdomen (Fig. 3K). The sixth abdominal somite now

present, their posterodorsal margin straight andunarmed; lateral processes of somite V length about 2/3of somite VI length.

Uropod (Fig. 3K). Incompletely biramous; endopodas a small bud; exopod fused with protopod, with 6–7plumodenticulate setae along inner margin (distal setamay be very short) and small spine terminally.

Telson (Fig. 3K). The armature of posterior marginas in zoea II; telson length only slightly exceeds theirwidth; anal spine absent.

Zoea IVDuration. 6–8 days.Size. CL = 2.82 ± 1.13 mm (2.59 – 3.04 mm,

N = 15).

Carapace (Fig. 4A). No remarked changes.Antennule (Fig. 4B). Protopod with 3 long plumose

setae at the base of endopod and 3–4 simple setae at thebase of exopod; endopod bud unarmed, with acute tip;exopod with 9 aesthetascs placed in three tiers (4, 2, 3)and 4 simple terminal setae.

Antenna (Fig. 4C). Endopod somewhat longer thanscaphocerithe; scaphocerithe length opposite their widthequal 7; otherwise unchanged.

Mandible (Fig. 4D). Palp present as a bud.Maxillule (Fig. 4E). Endopod unchanged; coxal

endite with 6 plumodenticulate setae marginally plus 2short simple setae submarginally; basial endite with 6marginal elongate cuspidate setae armed with few smalldenticles plus 2 submarginal simple setae.

Maxilla (Fig. 4F). Coxal endite with 6 (rarely 7)marginal + 1 submarginal plumodenticulate setae onproximal lobe; scaphognathite with 16 marginal plu-mose setae; unarmed proximal lobe of scaphognathitenow well separated from protopod; otherwiseunchanged.

Maxilliped I (Fig. 4G). Exopod with 8 terminalplumose natatory setae; otherwise unchanged.

Maxilliped II (Fig. 4H). Unchanged.Maxilliped III (Fig. 4I). Endopod with 1 terminal

plus 1 subterminal simple setae; exopod with 8 terminalplumose natatory setae.

Pereopods (Fig. 4J). Incompletely segmented;pereopod I chelated.

Abdomen (Fig. 4K). Second to fifth somites withuniramous pleopods.

Uropod (Fig. 4K). Endopod bud fused withprotopod, with a terminal simple seta; exopod separatedfrom protopod, with 6–7 plumodenticulate setae alonginner margin and bifid spine terminally.

Telson (Fig. 4K). Two pairs simple setae dorsally;length increased; otherwise unchanged.

MegalopaDuration. Undetermined.Size. CL = 1.38 ± 0.11 mm (1.24 – 1.53 mm, N = 7).Carapace (Fig. 5A, AN). Rostrum short, protuberant,

right-angled, with some pairs of simple setae on itssurface. Carapace surface with numerous groups ofsimple setae, 10 plumose setae along the both side offrontal margin, 10–11 plumose setae along each ofposteriolateral margin. Ocular peduncles with 3 dorsaland 1 lateral simple setae.

Antennule (Fig. 5B). Biramous; peduncle 3-segmented, over-reaching ocular peduncles; eachsegment with 5–6 simple setae, proximal segment withadditional 5 small plumose setae; endopod 2-segmented,proximal segment with 5 simple setae and distal

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Fig. 4. Pagurus gracilipes, zoea IV. A, lateral view; B, antennule; C, antenna; D, mandibles; E, maxillule; F, maxilla;G, maxilliped I; H, maxilliped II; I, maxilliped III; J, pereopods; K, ventral view of abdomen (posterodorsal setae on thesomites III–V are omitted).

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Fig. 5. Pagurus gracilipes, megalopa. A, dorsal view; AN, details of rostrum; B, antennule; C, antenna; D, mandibles;E, maxillule; F, maxilla; G, maxilliped I; H, maxilliped II; I, maxilliped III.

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Fig. 6. Pagurus gracilipes, megalopa. A, left cheliped; B, right cheliped; C, pereopod II; D, pereopod III; DN, details ofpereopod III; E, pereopod IV; EN, details of pereopod IV.

segment with 9 (4 terminal and 5 subterminal) simplesetae; exopod 4-segmented, proximal segment unarmed;the second segment with 7 aesthetascs + 1 long simpleseta; the third with 4 aesthetascs + 1 long and 3 shortsimple setae; the fourth with 3 aesthetascs + 4 terminal

(3 short and 1 long) setae; distal segment longer than thefirst three combined.

Antenna (Fig. 5C). Longer than pereopod I. Peduncle5-segmented, each segment with some simple setae;acicle terminating acutely, with 4 subterminal and 2–3

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Fig. 7. Pagurus gracilipes, megalopa. A, dorsal view of abdomen; B, left uropod; C, right uropod; D–G, pleopods I–IV.

lateral simple setae; flagellum 20–23-segmented, eachsegment with 0–5 simple setae, for the exception of thedistal segment (4 terminal and 4–6 subterminal setae).Mandible (Fig. 5D). Reduced and simplified, withshallow folds on surface; palp 2-segmented, terminalsegment with 7 short setae.

Maxillule (Fig. 5E). Endopod unsegmented, un-armed, sometimes with 1 submarginal seta; 1 smallplumose seta lower the base of endopod; coxal enditewith 7–8 setae and 3–5 small teeth; basial endite with12–14 marginal cuspidate setae, 4 marginal, 2 sub-marginal and 2 lateral plumodenticulate setae.

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Maxilla (Fig. 5F). Endopod unsegmented, with 1submarginal simple seta; proximal and distal lobes ofcoxal endite with 6 and 5 setae, respectively; proximaland distal lobes of basial endite with 8–9 and 11–12setae, respectively; scaphognathite with 42–45 marginalplumose setae and 5 simple setae on the surface.

Maxilliped I (Fig. 5G). Endopod reduced, unseg-mented, with 2 lateral plumose setae and 1–2 terminalshort setae; coxa with 5–7 setae (some of themplumose); basis with 15–17 setae; exopod reduced,incompletely 2-segmented, with 1 simple subterminalseta and 0–3 terminal short setae.

Maxilliped II (Fig. 5H). Endopod 4-segmented, with0–1, 0–1, 3–4, 4–5 setae; coxa with 1 plumose seta;basis unarmed; exopod incompletely 2-segmented,proximal part with 1 simple seta, distal part with 4terminal and 1 subterminal plumose setae.

Maxilliped III (Fig. 5I). Endopod 5-segmented; firstsegment with 6–7 simple setae and 2 small blunt teeth;second segment with 3–5 simple setae and 1 tooth;following three segments with 7–10, 24–25 and 14–15simple and plumodenticulate setae, respectively; coxaunarmed; basis with 1 simple seta; exopod incompletely2-segmented; proximal part with 1 simple and 1 plu-mose setae, distal part with 4–5 terminal and 1 sub-terminal plumose setae.

Pereopods (Fig. 6A–EN). The surface of segments ofall pereopods covered with simple setae of differentlength. Right chela slightly larger than left one; dactyliof pereopods II and III longer than propodi. Propodus ofpereopod IV with rasp of 6–7 corneous scales and 9–10simple setae; dactylus tip as a small claw, dactylussurface with 0–3 small corneous scales and 8–9 simplesetae. Propodus of pereopod V with rasp of 11 corneousscales, 6–8 simple setae and 8 long curved serrate setae.Dactylus with up to 12 corneous scales of different sizeand about 10 simple setae.

Abdomen (Fig. 7A). Consist of six somites; dorsalsurface with numerous simple setae; second throughfifth somites with biramous pleopods; sixth somite witha pair of uropods.

Pleopods (Fig. 7D–G). Biramous; endopods of pleo-pods I–III with 3 terminal hooks, endopod of pleopod IVwith 2 hooks; exopods of pleopods I–IV with 11, 11,9–11 and 9 plumose natatory setae, respectively.

Uropod (Fig. 7B, C). Biramous, asymmetrical; theleft uropod somewhat larger than right one; endopodwith 5–6 corneous scales and 4 simple setae (1 of themterminal); exopod with 14–15 corneous scales, 12plumose and 5–6 simple setae along the margin and 2simple setae on the surface.

Telson (Fig. 7A). Ovoid, slightly asymmetrical, withnumerous small simple setae on dorsal surface and 8long plumose setae along posterior margin.

Discussion

The genus Pagurus currently contains well over100 species and it needs to be completely revised (Ingle,1985). Because of its recognized heterogeneity, speciesof this genus have been divided into informal groupsbased either on the adult or larval morphology. Based onthe similarities of larval characters, four groups (A–D)were distinguished (see Roberts, 1970; McLaughlin andGore, 1988). Ingle (1985) proposed a classification(subdivisions I and II) including both adult and larvalfeatures, with subdivision II generally corresponding tothe larval group A.

Aсcording to their larval characters most of thehermit crabs inhabiting Russian waters of the Sea ofJapan (Pagurus brachiomastus, P. ochotensis, P. mid-dendorffii, P. proximus, P. pectinatus, P. minutus) arethe members of Group A (typical representative:Pagurus bernhardus) (Hong, 1981; Konishi andQuintana, 1987, 1988; Quintana and Iwata, 1987;McLaughlin and Gore, 1988; Kim and Hong, 2005;Kornienko and Korn, 2006). They possess a narrowtelson (telson seta IV in zoea III–IV is longer than one-half telson width), antennal endopod lacking setae,scaphocerite of antenna straight, with #8 plumose setaein all zoeal stages, length:width ratio $6, mandibularpalp appearing in zoea IV, endopods of uropods lackingsetae, antenna of megalopa longer than pereopod I. Onlytwo characters do not coincide with this classification:zoeal telson seta IV in all species listed above isarticulated (not fused) but lateral processes in somite Vare of different length, the longest being in P. ochotensis(Quintana and Iwata, 1987). Furthermore, according tosubdivision II (Ingle, 1985), zoeal telson seta III of allspecies is not reduced from stage III and antennalflagellum of megalopa extends beyond the chela.

The larval characters of P. gracilipes considerablydiffer from the morphological features of all otherpagurids inhabiting the Russian waters of the Sea ofJapan. On the basis of cheliped morphology and otherattributes of the adult, P. gracilipes appears the mostclosely related to McLaughlin’s (1974) “bernhardusgroup” of Pagurus (Lemaitre and McLaughlin, 2003),or, according to larval features studied by Ingle (1985),belonging to subdivision II. However, detailed descrip-tion of their larvae suggests that P. gracilipes shouldrather to be placed in Group C (typical representative:Pagurus anachoretus) or Ingle’s (1985) subdivision I.Zoeae of P. gracilipes possess broad telson, telson setaIV articulated, in zoea III it is slightly longer and in zoeaIV approximately equal to one-half telson width,antennal endopod with 2 plumose setae in zoea I, but 1simple setae in zoea III–IV, antennal scaphoceritecurved, with 10 setae in all zoeal stages, length:width

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Table 1. Morphological differences for appendages of zoea of three pagurid species

Feature Pagurus kulkarnii (Tirmizi andSiddiqui, 1980, after figures)

Pagurus constans(Hong and Kim, 2002)

Parapagurodes hartae(McLaughlin and Jensen, 1996)

Zoea IAntennuleendopod 1 1 1 exopod 2 aesthetascs+3 setae 5 aesthetascs 2–3 aesthetascs+3–4 setaeAntennaprotopodal spine 1 1 1endopod 2 0 0scaphocerite 9 6 9Maxilluleendopod 1, 0, 3 2, 1, 3 1–2, 1, 3coxal endite 6 2+5 6basial endite 2 2+2 2+2Maxillaendopod 3+3 3+4 (2–3)+4coxal endite (1+4)+(1+3) (1+6)+(1+3) (1+5)+(1+3)basial endite (1+4)+(1+3) (1+4)+(1+3) (1+4)+(1+3)scaphognathite 5 5 5Maxilliped Iendopod 3, 2, 1, 2, 4+I 3, 2, 1, 2, 4+I 3, 2, 1, 2, 4+Ibasis 1, 2, 3, 3 2, 2, 3, 3 1–2, 2, 2–3, 2–3exopod 4 4 4Maxilliped IIendopod 2, 2, 2, 4+I 2, 2, 2, 4+I 2, 2, 2, 4+Ibasis 2 1, 2 1, 2exopod 4 4 4Zoea IIAntennuleendopod 1 1 exopod 3 aesthetascs+2 setae 5 aesthetascsAntennaprotopodal spine 1 1endopod 2 0scaphocerite 9 7Maxilluleendopod 0, 0, 4 2, 1, 3coxal endite 5 2+5basial endite 4 2+4Maxillaendopod 2+3 3+4coxal endite (1+6)+(1+3) (1+6)+(1+3)basial endite (1+4)+(1+3) (1+4)+(1+3)scaphognathite 7 7Maxilliped Iendopod 3+I, 2+I, 1+I, 2, 4+I 3+I, 2+I, 1+I, 2, 4+Ibasis 1, 2, 3, 3 2, 2, 3, 3exopod 7 7Maxilliped IIendopod 2, 2+I, 2+I, 4+I 2, 2+I, 2+I, 4+Ibasis 1, 2 1, 2exopod 7 7Maxilliped IIIendopod 2 2exopod 6 6Zoea IIIAntennuleprotopod 2+2 1+2 endopod 1 1 exopod 4 aesthetascs+1 seta 8 aesthetascs

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E.S. Kornienko and O.M. Korn / IRD 50 (2007) 31–46 43

Feature Pagurus kulkarnii (Tirmizi andSiddiqui, 1980, after figures)

Pagurus constans(Hong and Kim, 2002)

Parapagurodes hartae(McLaughlin and Jensen, 1996)

Antennaprotopodal spine 2 2endopod 0 1scaphocerite 9 7Maxilluleendopod 1, 0, 4 2, 1, 3coxal endite 6 2+5basial endite 4+2 2+4Maxillaendopod 2+3 3+4coxal endite (1+6)+(1+3) (1+5)+(1+3)basial endite (1+4)+(1+3) (1+4)+(1+3)scaphognathite 9 10–11Maxilliped Iendopod 3+I, 2+I,1+I, 2+I, 4 3+I, 2+I, 1+I, 2, 4+Ibasis 1, 2, 3, 3 2, 2, 3, 3exopod 7 7Maxilliped IIendopod 2, 2+I, 2+I, 4+I 2, 2+I, 2+I, 4+Ibasis 1, 2 1, 2exopod 7 7Maxilliped IIIendopod 2 2exopod 7 7Uropodendopod 0 0exopod 7 5Zoea IVAntennuleprotopod 3+1 1+2 endopod 1 0exopod 7 aesthetascs+3 setae 10 aesthetascsAntennaprotopodal spine 2 2endopod 2, 1, 4, 0 1scaphocerite 9 7Mandible (palp) absent presentMaxilluleendopod 0, 1, 3 2, 1, 3coxal endite 7 2+6basial endite 5 2+6Maxillaendopod 3+3 2+4coxal endite (1+5)+(1+3) (1+6)+(1+3)basial endite (1+4)+(1+3) (1+4)+(1+3)scaphognathite 16 12Maxilliped Iendopod 3+I, 2+I, 1, 1+I, 4 3+I, 2+I, 1+I, 2, 4+Ibasis 1, 1, 3, 2 2, 2, 3, 3exopod 8 8Maxilliped IIendopod 2, 2+I, 2+I, 4+I 2, 2+I, 2+I, 4+Ibasis 1, 2 1, 2exopod 7 8Maxilliped IIIendopod 2 3exopod 8 8Uropodendopod 2 0exopod 7 5

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ratio from 5 (in zoea I) to 7 (in zoea IV), endopods ofuropods with 1 seta. However, the larvae of this speciesshare 3 larval characters with representatives ofGroup A: long lateral processes in somite V (but manyrepresentatives of Group A have lateral processes ofmedium length), the presence of mandibular palp inzoea IV and the length of antenna in megalopa (it islonger than pereopod I).

Only two species, P. anachoretus and P. kulkarnii,have been previously assigned to Group C (McLaughlinand Gore, 1988). The larvae of P. anachoretus weredescribed briefly (Pike and Wiliamson, 1960) and it isnot possible to compare the morphology of P. ana-choretus and P. gracilipes in detail. Zoeae and mega-lopa of P. kulkarnii were described more thoroughly(Shenoy, 1967; Tirmizi and Siddiqui, 1980). Zoeae ofP. kulkarnii and P. gracilipes have a small dorsal longi-tudinal keel on the carapace. The larvae of both speciesshare antennular and antennal setation with the excep-tion of antennal endopod of zoea II: P. kulkarnii has2 plumose setae, but P. gracilipes is unarmed. Bothspecies have wide curved scaphocerite. At the sametime, zoeae of P. gracilipes are slightly distinguishedfrom those of P. kulkarnii in setation of maxillule,maxilliped III, basis of maxilliped I; zoea IV in P.kulkarnii has no palp bud. In larvae of P. gracilipesendopods of uropods have 1 seta, whereas in those ofP. kulkarnii there is 1 seta (Shenoy, 1967), or 2 (Tirmiziand Siddiqui, 1980). Thus, the general larval featuresallow us to assign P. gracilipes as well as P. kulkarnii toGroup C of Pagurus larvae.

At present, the genus Parapagurodes comprises onlytwo species: P. makarovi and P. laurentae (McLaughlinand Asakura, 2004). In both, only telsons of prezoea aredescribed (McLaughlin and Haig, 1973). Consequently,we have no opportunity to compare the larvae ofPagurus species with those of Parapagurodes, to definethe characteristic features of this genus and to clarify thetaxonomic position of P. gracilipes.

Among the species previously referred to the genusParapagurodes, complete larval development has beendescribed in P. constans (Hong and Kim, 2002). Inaddition, zoea I has been illustrated in P. hartae(McLaughlin and Jensen, 1996).

The comparison of larval P. gracilipes with those inP. constans and P. hartae shows that zoeae of thesespecies differ considerably (Table 1). According toRoberts (1970), P. constans and P. hartae larvae aremore closely related to Group A of Pagurus larvae.They have narrow telson with telson seta IV more thanone-half telson width; antennal endopod lack setae. In P.hartae scaphocerite of antenna is straight and has 7plumose setae; in P. constans it has 6–7 setae; itslength:width ratio is $6 in both species. Mandibular

Table 2. Morphological differences for appendages of mega-lopa of two pagurid speciesFeature Pagurus kulkarnii

(Tirmizi andSiddiqui, 1980,after figures)

Pagurus constans(Hong and Kim,2002)

Antennulapeduncle 7, 3, 1 unknownendopod 3, 6 2, 6exopod 0, 3, 3, 5

aesthetascs;0, 0, 1, 3 setae

0, 3, 3, 2aesthetascs;0, 0, 2, 4 setae

Antennaacicle 3 3flagellum 7-segmented 10-segmentedMandible (palp) 0 0, 2–4Maxillulaendopod 0 0coxal endite 6 10 basial endite 12 spines + 1 seta 11–12 spines +

2–3 setae Maxillacoxal endite 4+4 5+4basial endite 6+6 7+5scaphognathite 24–26 28–30Maxilliped Iendopod 0 4coxa 1 3basis 12 17–18exopod 2 6Maxilliped IIendopod 0, 0, 0, 4 0, 0, 1, 3basis 1 0exopod 0, 5 0, 6Maxilliped IIIendopod 1, 4, 3, 6, 8 numerousbasis 0 unknownexopod 0, 6 0, 5Uropodendopod 2–3 corneous

scales + 2–3 setae3 corneous scales+ 3–4 setae

exopod 4–6 corneousscales + (5–6) +(2–3) setae

9 corneous scales+ 11–12 setae

Pleopodsendopod 2 hooks 2 hooksexopod 8–9 8–9

palp in P. constans appears in zoea IV; endopods ofuropods of this species lack setae; antenna of megalopais longer than pereopod I. P. constans is similar tospecies of Group C only in two features: antennalscaphocerite of this species is curved, and lateralprocesses are of medium length (but, as mention above,the latter in Group A is variable).

Moreover, zoeae of P. constans and P. hartae aredistinguished from those of P. gracilipes by morphology

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of antennae: scaphocerite in both the former has only6–7 plumose setae, whereas in P. gracilipes scapho-cerite has 10 setae. P. constans and P. gracilipes have asimple antennal endopod, whereas P. hartae has a bifidone. A bifid antennal endopod was earlier recorded alsofor P. minutus (Hong, 1981), P. geminus (Konishi andQuintana, 1988), and P. trigonocheirus (Quintana andIwata, 1988). Antennular protopod of P. constans has1 plumose seta in zoeae III–IV, but P. gracilipes has2 setae in zoea III and 3 in zoea IV. Endopods ofmaxilliped III of P. constans have 2, 2, 3 setae in zoeaeII–IV, respectively, but endopods of P. gracilipes haveonly 1, 1, 2 setae, respectively. The pair of posterodorsalsetae on abdominal somites II–V found in P. constans ispresent also in P. gracilipes. The first telson seta in P.constans and P. gracilipes is fused, whereas in Para-pagurodes makarovi, P. laurentae (McLaughlin andHaig, 1973) and P. hartae (McLaughlin and Jensen,1996) it is articulated. It is interesting that zoea I ofP. hartae possess a short, low keel in the dorsal midlineof the carapace, similar to the dorsal keel of P. graci-lipes and P. kulkarnii. A unique character of zoea IV inP. gracilipes is the presence of 2 pairs of simple dorsalsetae on the telson.

Numerous differences are also found in megalopalsetation of the considered species (Table 2). However,the lacking of classification of pagurid megalopae doesnot allow us to assign P. gracilipes megalopa to one ofthe larval divisions. However, we note that megalopa ofthis species possess some features not recorded in otherpagurid species inhabiting Russian waters of the Sea ofJapan: a broad rostrum with straight front margin, asmall plumose seta on the inner side of maxillula, setaeon the surface of uropods and 5 simple setae on thesurface of the maxillar scaphognathite.

Thus, although P. gracilipes, P. hartae, and P. con-stans were earlier assigned to the genus Parapagurodeson the basis of adult characters, their larvae represent aheterogeneous group and should evidently be placed todifferent subdivisions of Pagurus larvae.

Acknowledgements

The project was partially supported by the Far EastBranch of Russian Academy of Sciences (grants no. 06-III-А-06-164 and 06-III-Д-06-238) and by the RussianFound of Fundamental Researches (grants no. 06-04-96039 and 06-04-630092).

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