The Larval Development of the Hermit Crab Areopaguristes Nigroapiculus (Decapoda: Anomura: Diogenidae) Reared Under Laboratory Conditions Elena S

Journal of the Marine Biological Association of the United Kingdom, 2011, 91(5), 1031–1039. # Marine Biological Association of the United Kingdom, 2011 doi:10.1017/S0025315410002225 The larval development of the hermit crab Areopaguristes nigroapiculus (Decapoda: Anomura: Diogenidae) reared under laboratory conditions elena s. kornienko and olga m. korn A.V. Zhirmunsky Institute of Marine Biology, Far East Branch, Russian Academy of Sciences, 17 Pal’chevskogo Street, 6900041, Vladivostok, Russia

The larval development of the hermit crab Areopaguristes nigroapiculus (Komai, 2009) (Decapoda: Anomura: Diogenidae) is described and illustrated from the material reared in the laboratory. The development included three zoeal and a single megalopal stages. At 22–258C, megalop of A. nigroapiculus was attained 6–9 days after hatching. The present paper is the ﬁrst description of the complete larval development in the genus Areopaguristes. Morphological characters of zoeas and megalop of A. nigroapiculus are compared with those described for the closely related Paguristes species. The comparison on the zoeal characters revealed that A. nigroapiculus is distinguished from Paguristes species by the absence of anterolateral carapace spines and by the fused fourth telson process in zoea III. These two features are possible generic characters of Areopaguristes. In the rest of larval characters, A. nigroapiculus agree well with Paguristes species having three zoeal stages. In the plankton of Peter the Great Bay, the larvae of A. nigroapiculus sporadically occurred only in July and August, at depths of 3–45 m and surface water temperatures of 18–228C.

Keywords: Decapoda, Anomura, Diogenidae, Areopaguristes nigroapiculus, larva, Sea of Japan

Submitted 2 June 2010; accepted 29 November 2010; ﬁrst published online 1 February 2011

INTRODUCTION At present, the genus Areopaguristes is represented by 22 species (Komai, 2009). Among these species the larvae of The species of the genus Paguristes Dana, 1851 was primarily only A. abbreviatus (Dechance´, 1963) were previously described as having 13 pairs of gills. Later it was found that in described (see Dechance´, 1963). However, this species has a several Paguristes species the gill number was reduced to direct larval development; they hatch as megalopal stage. 12 (Rahayu, 2005). Rahayu (2005) reinstated the genus The aim of this study is to give a description of the com- Stratiotes, originally established by Thomson (1899), because plete larval development of A. nigroapiculus based on the lab- the type species had only 12 pairs of gills. In recent studies, oratory reared material. It is the first illustration of non-direct species having this character and previously assigned to larval development in species of the genus Areopaguristes.As Paguristes were transferred to Stratiotes and several new the genera Areopaguristes and Paguristes are closely related to Stratiotes species were also described (Rahayu, 2005, 2007; each other, we have tried to compare the larval characters of Parente & Hendrickx, 2006; Komai, 2009). Areopaguristes nigroapiculus and Paguristes species. In August 2004, a new representative of warm-water hermit crabs was found in Peter the Great Bay (Russian waters of the Sea of Japan) and it was identified as MATERIALS AND METHODS Paguristes ortmanni Miyake, 1978 (see Petryashov & Kornienko, 2006). Subsequent to this publication we sent An ovigerous female of Areopaguristes nigroapiculus was col- some specimens of this hermit crab to Dr Tomoyuki Komai lected from Vostok Bay (inner bay of Peter the Great Bay, Sea (Natural History Museum and Institute, Chiba, Japan) for of Japan) in July 2004, at a depth of about 3 m. The female was confirmation of the identification. As a result, it was found maintained in an aquarium with aerated seawater until hatch- to be actually a new species—Stratiotes nigroapiculus Komai, ing of the larvae. Hatching larvae were concentrated at the 2009 occurring also from Hokkaido to Sagami Bay and to edge of aquarium using a point-light source and transferred Akita Prefecture in Japan, subtidal to 140 m (Komai, 2009). to 1-l glass vessels with filtered and UV-sterilized seawater The name of the genus Stratiotes is now replaced by and reared to the megalopal stage at temperatures of 22– Areopaguristes by Rahayu & McLaughlin (2010). 258C and a salinity of 32‰. The density of the larvae was about 100 specimens per litre. The larvae were fed newly

Corresponding author: hatched nauplii of Artemia sp. The water in the vessels was E.S. Kornienko changed daily. The larval development was evaluated twice a Email: [email protected] day.

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The larvae were fixed in 4% formaldehyde for light micro- and with 2 submarginal simple setae; endopod 3-segmented, scopic studies. The fixed larvae were dissected under a proximal segment with 1 short simple seta, median segment MBS-10 stereomicroscope using fine entomological needles. with 1 long plumodenticulate seta, distal segment with 3 The outlines of the larvae and their appendages of different long terminal plumodenticulate setae. developmental stages were drawn using a camera lucida Maxilla (Figure 1G): coxal and basial endites each bilobed; attached to a binocular Ergaval microscope (Carl Zeiss coxal endite with 5 or 6 marginal and 1 submarginal setae on Jena). Respective measurements were made with an ocular proximal lobe and with 3 marginal and 1 submarginal setae on micrometer. Methods of measurements, descriptions of setal distal lobe; basial endite with 4 marginal and 1 submarginal arrangements and terminology followed that of Clark et al. setae on proximal lobe and 3 marginal and 1 submarginal (1998) and Konishi & Shikatani (1998). The setal arrange- setae on distal lobe; all setae on coxal and basial endites plu- ments are listed from protopod or coxal endite to exopod, modenticulate; endopod unsegmented, with 8 plumodenticu- from proximal to distal segments, and from anterior to pos- late setae in 3 tiers (3 + 2 + 3); scaphognathite fused with terior pleonal somites. The carapace length (CL) was protopod in proximal part, distal lobe with 5 marginal measured from the tip of the rostrum to the posterior mid- plumose setae. point of the carapace. Maxilliped I (Figure 1H): coxa with 1 plumodenticulate Specimens of larval stages and the spent female are depos- seta; basis with setal formula 2, 3, 3, 3; endopod 5-segmented, ited in the Museum of the Institute of Marine Biology, Russian setal formula progressing distally 3, 2, 1, 2, 4 + I plus numer- Academy of Sciences, Vladivostok (accession number 22933). ous thin setae on first to third segments; exopod 2-segmented, The seasonal occurrence of larvae of A. nigroapiculus in with 4 terminal plumose natatory setae. Peter the Great Bay was studied using the material of plankton Maxilliped II (Figure 1I): coxa without setae; basis with surveys, twice a month from April to October 2007 and 2008. setal formula 1, 2; endopod 4-segmented, setal formula pro- A Juday net with a ring diameter of 38 cm and a filtering cone gressing distally 2, 2, 2, 4 + I, numerous thin setae on made of a 168 mm mesh was used. Samples were taken at 66 second and third segments; exopod as in first maxilliped. stations across the entire water column from the bottom to the Maxilliped III (Figure 1J): biramous, without setae. surface at depths ranging from 2 to 75 m. Simultaneously the Pereiopods: visible as small buds, first pereiopod bilobed. temperature was measured at the water surface. Pleon (Figure 1A, K): consisting of 5 somites and telson. Somite 2 with 1 prominent mediodorsal spine; somites 3 and 4 each with 1 short mediodorsal spine; somite 5 with 1 RESULTS prominent mediodorsal and 1 pair of lateral spines, 1 fine seta present at base of each lateral spine. Description Telson (Figure 1A, K): fan-shaped, nearly as long as wide; posterior margin with median cleft and with 7 + 7 processes: Areopaguristes nigroapiculus hatched at a prezoea, which first (outermost) process showing a short smooth articulated lasted about half an hour before moulting to the zoea I. It spine, second process a short plumose anomuran hair, third then passed three zoeal stages. The time required to reach to seventh processes plumodenticulate articulated setae, the megalopal stage was 6–9 days at temperatures of 22–258C. fourth process longest; posterior margin also covered with short setules, few long setules in median cleft; small anal Areopaguristes nigroapiculus (Komai, 2009) (Figures 1–5) spine present. Coloration in life: body generally translucent; dorsal surface zoea i of carapace and pleon with red-black chromatophores (as Duration: 2–3 days. shown in Figure 1A); dorsal surface of telson with violet chro- Size:CL¼ 0.90 + 0.04 mm (0.84–0.94 mm, N ¼ 13). matophores (as shown in Figure 1K), ventral surface with Carapace (Figure 1A, B): no setae on surface, low keel ante- yellow-brown chromatophores; basis of maxilliped I with red- riorly in dorsal midline; rostrum short, tapering, not exceed- brown chromatophore, endopod and exopod each with red- ing 1/3 length of carapace, nearly equal in length to brown chromatophores; endopod and exopod of maxilliped antennular exopod but shorter than antennal scaphocerite; II with red-brown chromatophores (as shown in Figure 1H, posterolateral margins rounded; eyes sessile. I); ventral surface of body with red chromatophores at base Antennule (Figure 1C): uniramous, with 3 terminal aesthe- of mandibles. tascs of different lengths, 3 short terminal sparsely plumose setae, and 1 long subterminal densely plumose seta. zoea ii Antenna (Figure 1D): biramous; endopod fused with proto- Duration: 2–3 days. pod, bearing 3 (2 long and 1 short) terminal plumose setae; Size:CL¼ 0.99 + 0.04 mm (0.90–1.05 mm, N ¼ 10). protopod with 1 strong serrate spine near junction with Carapace (Figure 2A, B): eyes stalked, otherwise as in endopod; scaphocerite longer than endopod and about 4 zoea I. times longer than wide, with a distal strong spine, 9 long Antennule (Figure 2C): biramous; protopod with 1 short plumose setae and 1 short distal simple seta. seta at distal end; endopod and exopod clearly separated Mandibles (Figure 1E): asymmetrically dentate; incisor from protopod; endopod with 1 long terminal plumose seta; process with a single strong tooth and few small teeth; exopod with 6 or 7 terminal aesthetascs and 3 terminal molar process with serrate ridges and small acute denticles; plumose setae. no palp buds. Antenna (Figure 2D): biramous; protopod with 2 spines Maxillule (Figure 1F): coxal endite with 7 (5 marginal and 2 (1 strong serrate, 1 short smooth) on distal margin; submarginal) plumodenticulate setae; basial endite with 2 endopod separated from protopod; scaphocerite as in zoea I. marginal, elongated spine-like teeth bearing small denticles Mandibles (Figure 2E): palps present as buds.

Fig. 1. Areopaguristes nigroapiculus, zoea I. (A) Dorsal view; (B) lateral view; (C) antennule; (D), antenna; (E) mandibles; (F) maxillule; (G) maxilla; (H) maxilliped I; (I) maxilliped II; (J) maxilliped III; (K) pleon, dorsal view.

Maxillule (Figure 2F): coxal endite and endopod as in zoea Carapace (Figure 3A, B): as in zoea II. I; basial endite with 4 marginal elongated spine-like teeth Antennule (Figure 3C): protopod incompletely 3- bearing small denticles and with 2 submarginal simple setae. segmented, with 2 long plumose setae and 3 short simple Maxilla (Figure 2G): coxal and basial endites, endopod as in setae at distal margin; endopod with 1 terminal plumose seta; zoea I; scaphognathite with 7 marginal plumose setae. exopod with 8 aesthetascs in 2 tiers and 3 short terminal setae. Maxilliped I (Figure 2H): coxa and basis as in zoea I; Antenna (Figure 3D): protopod as in zoea II; endopod endopod setal formula progressing distally 3 + I, 2 + I, 1 + incompletely segmented, with 2 terminal short setae; scapho- I, 2, 4 + I; exopod with 7 terminal plumose natatory setae. cerite with 10 plumose setae. Maxilliped II (Figure 2I): coxa and basis as in zoea I; Mandibles (Figure 3E): palp buds increasing in size. endopod setal formula progressing distally 2, 2 + I, 2 + I, Maxillule (Figure 3F): coxal endite with 9 marginal plumo- 4 + I; exopod with 7 terminal plumose natatory setae. denticulate setae; basial endite with 5 or 6 marginal and sub- Maxilliped III (Figure 2J): biramous; endopod with 2 or 3 marginal spine-like elongated teeth bearing small denticles plumodenticulate setae; exopod incompletely 2-segmented, and with 2 submarginal simple setae; endopod as in previous with 6 or 7 terminal plumose natatory setae. stages. Pereiopods (Figure 2K): unsegmented, distinctly chelate. Maxilla (Figure 3G): coxal and basial endites, endopod Pleon (Figure 2A, B): as in zoea I. usually as in zoea II (number of setae on proximal lobe of Telson (Figure 2A, L): median cleft absent; few long setules coxal endite sometimes increasing up to 8); proximal lobe of replaced by a small spine; posterior margin covered with short scaphognathite without setae, now well separated from proto- setules, with 8 + 1 + 8 processes; anal spine inconspicuous. pod, distal lobe with 8 or 9 marginal plumose setae. Maxilliped I (Figure 3H): unchanged from zoea II. zoea iii Maxilliped II (Figure 3I): unchanged from zoea II. Duration: 2–3 days. Maxilliped III (Figure 3J): exopod with 7 terminal plumose Size:CL¼ 1.11 + 0.04 mm (1.03–1.14 mm, N ¼ 12). natatory setae; otherwise as in zoea II.

Fig. 2. Areopaguristes nigroapiculus, zoea II. (A) Dorsal view; (B) lateral view; (C) antennule; (D) antenna; (E) mandibles; (F) maxillule; (G) maxilla; (H) maxilliped I; (I) maxilliped II; (J) maxilliped III; (K) pereiopods; (L) telson, dorsal view.

Pereiopods (Figure 3K): increasing in size but incompletely penultimate segment with 4 or 5 setae, ultimate segment segmented; first pereiopod chelate. with 3 setae; endopod 2-segmented, proximal segment with Pleon (Figure 3A, L): sixth somite now delineated, with 1 simple seta, distal segment with 7 simple setae; exopod 2- small mediodorsal spine; second to fifth somites each with a segmented; proximal segment without setae; distal segment pair of small, biramous pleopod buds. with 5 or 6 subterminal aesthetascs, 1 long terminal and 7 Uropod (Figure 3L, M): endopod as a small bud; exopod or 8 short subterminal simple setae. fused with protopod, with 8 plumose setae on inner margin Antenna (Figure 4D): shorter than cheliped; peduncle 3- and a smooth, long terminal spine. segmented, with 4 or 5, 1 or 2, 2 or 3 simple setae; flagellum Telson (Figure 3M): posterior margin with 9 + 9 processes; 4-segmented; first segment without setae; second segment fourth process comparatively shorter than in zoea II, fused to with 0–2 short simple setae; third segment with 6 long telson; marginal setules present. simple setae, fourth segment with 8 or 10 long simple setae; antennal acicle terminating acutely, with 2 subterminal megalop spines and 3 subterminal simple setae. Duration: undetermined. Mandibles (Figure 4E): simplified, palps 3-segmented, Size:CL¼ 0.65 + 0.02 mm (0.61–0.68 mm, N ¼ 12). terminal segment with 4 or 5 short setae. Carapace (Figure 4A, B): dorsal surface covered with sparse Maxillule (Figure 4F): coxal endite with 3 short setae and 3 simple setae, with 7 setae along each posterolateral margin; or 5 minute teeth; basial endite with 7 marginal teeth, 3 or 4 rostrum small, inconspicuous; ocular acicles absent; ocular plumodenticulate and 3 simple setae; endopod reduced, peduncles longer than antennular peduncles, corneas subeq- unsegmented, without setae. ual in width to ocular peduncles. Maxilla (Figure 4G): coxal and basial endites bilobed; prox- Antennule (Figure 4C, C′,C′′): biramous; peduncle 3- imal lobe of coxal endite with 3 or 4 setae, distal lobe with 2 or segmented, with proximal segment bearing 6 or 7 (4 or 5 3 setae; proximal and distal lobes of basial endite with 4 or 5 plumose) setae and 1 small spine on distal margin, and 6 setae, respectively; endopod reduced, with 0–1 short

Fig. 3. Areopaguristes nigroapiculus, zoea III. (A) Dorsal view; (B) lateral view; (C) antennule; (D) antenna; (E) mandibles; (F) maxillule; (G) maxilla; (H) maxilliped I; (I) maxilliped II; (J) maxilliped III; (K) pereiopods; (L) pleon, ventral view; (M), telson, dorsal view.

seta on distall end; scaphognathite with 22 or 24 marginal segments with 7, 10 and 7 plumodenticulate or simple setae, plumose setae and 4 simple setae on surface. respectively; exopod incompletely 2-segmented, proximal Maxilliped I (Figure 4H): coxa with 3 simple setae; basis with part with 1 short median simple seta, distal part with 6 term- 16 simple or plumodenticulate setae; endopod and exopod inal plumose setae. reduced; endopod with 1 minute terminal seta or unarmed; Pereiopods (Figure 5A–F′): covered with scattered plumose exopod 2-segmented, proximal segment with 1 median and simple setae of different lengths. Chelipeds nearly equal; plumose seta, distal segment with 1 minute terminal seta. dorsal surfaces of carpus, propodus (palm) and dactylus Maxilliped II (Figure 4I): basis with 2 or 3 simple setae; covered with numerous minute setules; ischium with 1 small endopod 4-segmented, with setal formula progressing distally spine on ventral margin; merus with 3 spines on ventral 0–2, 0–1, 1–2, 2–3; exopod incompletely 2-segmented, with margin and 2 or 3 spines on dorsal margin, carpus with 2 proximal part bearing 1 short median simple seta, with distal spines on dorsodistal margin and 3 spines on dorsomesial part bearing 5 or 6 terminal plumose setae. margin; propodus with 3 spines on dorsomesial margin; dac- Maxilliped III (Figure 4J): basis with 2 or 4 simple setae; tylus with 1 proximal spine on mesial surface; dactylus and endopod 5-segmented, first segment with 2 or 3 simple fixed finger of both chelipeds each with a row of small teeth setae, second segment with 3 simple setae, following three along cutting edge, terminating in a corneous claw. In

Fig. 4. Areopaguristes nigroapiculus, megalop. (A) Dorsal view; (B) lateral view; (C) antennule; (C′) details of antennular endopod; (C′′) details of antennular exopod; (D) antenna; (E) mandibles; (F) maxillule; (G) maxilla; (H) maxilliped I; (I) maxilliped II; (J) maxilliped III.

pereiopod II (ﬁrst ambulatory leg), ischium with 1 minute Pleopods (Figure 5G): biramous; endopods each with 2 distal spine on both dorsal and ventral margins; merus with small hooks on distal margin; exopods each with 8 marginal 1 minute spine on ventral margin; carpus with 1–3 spines plumose setae. on dorsal margin; propodus with 1 distal spine on ventral Uropods (Figure 5H, H′): biramous, nearly symmetrical; margin; dactylus with 3 spine-like setae on ventral margin. endopod and exopod clearly separated from protopod; proto- In pereiopod III, carpus with 1 distal spine on dorsal pod with 1 long sparsely plumose seta, 1 short simple seta and margin; propodus with minute distal spine on ventral 1 small spine; endopod with 4 or 5 marginal corneous scales, 2 margin; dactylus with 2 or 3 spine-like setae on ventral or 3 long plumose and 3 or 4 short simple setae; exopod mar- margin. Carpi, propodi and dactyli of pereiopods II and III ginally with 8–11 corneous scales, 10 or 11 plumose setae, and covered with short transverse rows of minute setules. In per- 3 or 4 simple setae. eiopod IV, propodus has a rasp of 5 corneous scales on ventral Telson (Figure 5H, H′): nearly symmetrical, dorsal surface margin; dactylus terminating in a simple small claw. In pereio- with 2 rows of short simple setae along midline; posterior pod V, propodus has a rasp of 9 corneous scales and 2 or 3 margin rounded, with 10 long plumose setae, lateral long curved setae; dactylus has a rasp of 3 corneous scales; margins with some short simple setae. dactylus articulated with propodus subterminally. Coloration in life: carapace with 3 pairs of chromatophores Pleon (Figure 5H): consisting of six somites and telson; on dorsal surface; ocular peduncle with chromatophore on dorsal surface of all somites covered with simple setae as illus- dorsoproximal part; endopod and exopod of maxilliped II with trated; somites 2–5 each with biramous pleopods; somite 6 few chromatophores; telson with 2 pairs of chromatophores with uropods. on dorsal surface. All chromatophores are yellow-brown.

Fig. 5. Areopaguristes nigroapiculus, megalop. (A) Left cheliped, mesial view; (A′) left chela, dorsal view; (A′′) left chela, ventral view; (B) right cheliped, mesial view; (C) pereiopod II; (D) pereiopod III; (E) pereiopod IV; (E′) details of pereiopod IV; (F) pereiopod V; (F′) details of pereiopod V; (G) pleopod I; (H) pleon, dorsal view; (H′) telson and uropods, dorsal view.

Seasonal occurrence of larvae in the plankton from southern Australia; P. tortugae Schmitt, 1933 and P. erythrops Holthuis, 1959 from Brasilia; P. digitalis Stimpson, In the plankton of Peter the Great Bay, the larvae of 1858 and P. ortmanni Miyake, 1978 from the north-western Areopaguristes nigroapiculus occasionally occurred over Paciﬁc. depths ranging from 3 to 45 m, with maximal density of 1 3 Larval development in diogenid hermit crabs is highly vari- specimens/m . They were found only in July and August, able. Diogenids are well known to have abbreviated larval when surface water temperatures were 18–228C. development (Rabalais & Gore, 1989). Most Paguristes species have 3 zoeal and a megalopal stages, viz., P. turgidus (see Hart, 1937), P. digitalis (see Kurata, 1968), P. eremita DISCUSSION (see Pike & Williamson, 1960), P. spinipes (see Provenzano, 1978), P. erythrops (see Hebling & Fransozo, 1982), P. tortugae The genus Paguristes, which contains about 120 species in the (see Hebling & Negreiros-Fransozo, 1983) and P. ortmanni world, is the largest genus in the family Diogenidae (De Grave (see Quintana & Iwata, 1987). Paguristes sericeus has an et al., 2009; McLaughlin et al., 2010). However, the descrip- abbreviated development with only 2 zoeal stages (Rice & tions of larval developments are available for only nine Provenzano, 1965). In P. frontalis, larvae hatch at the megalo- species: Paguristes sericeus A. Milne-Edwards, 1880 and P. spi- pal stage, which indicates a direct larval development nipes A. Milne-Edwards, 1880 from West India; P. eremita (Morgan, 1987). As most members of the genus Paguristes, (Linnaeus, 1767) ¼ P. oculatus (Fabricius, 1775) from the Areopaguristes nigroapiculus has also 3 zoeal stages. Mediterranean Sea; P. turgidus (Stimpson, 1857) from the Based on our data, the larvae of A. nigroapiculus, as with north-eastern Paciﬁc; P. frontalis (H. Milne Edwards, 1836) most Paguristes species, attained the megalopal stage

approximately within one week after hatching. Only P. spi- Hokkaido (Asakura, 2006), so their larvae and the larvae of nipes (see Provenzano, 1978) possessed more prolonged A. nigroapiculus, may be simultaneously found in the plank- development: the megalopal stage of this species was attained ton sample in this region. The description of P. digitalis after 3–4 weeks after hatching. larvae by Kurata (1968) is not fully detailed. A comparison In our studies, the larvae of A. nigroapiculus are rarely of our material of A. nigroapiculus with the larvae of P. ort- encountered in Peter the Great Bay. Probably, this is due to manni (see Quintana & Iwata, 1987) indicated that the seta- that fact this species is not numerous in this area and its tion of appendages of both species are nearly identical in pelagic period is very short compared to other hermit crabs. zoea I and have slight differences in later zoeal stages. The zoea of A. nigroapiculus is smaller than any known Considerable distinctions are noted in the megalopal stage, Paguristes larvae. Carapace length of zoea I of A. nigroapiculus but they correspond to the usual differences between the is 0.9 mm, whereas that of the Paguristes species varies from larvae within one genus. 1.2 mm in P. digitalis to 1.9 mm in P. erythrops. Since the larvae of A. nigroapiculus, like Paguristes, have In the principal larval characters, A. nigroapiculus agrees only 3 zoeal stages, they represent accelerated development well with Paguristes species having 3 zoeal stages. In zoea, in comparison with the prolonged development of other these characters include: carapace with low keel anteriorly hermit crabs which comprise 4 or more zoeal stages. In A. on the dorsal midline; posterolateral margins of carapace nigroapiculus, the protopod of the antennule and endopod being rounded; short rostrum not extending as far as the of the antenna in zoea III are incompletely 3-segmented; the antennular exopod and antennal scaphocerite; scaphocerithe mandibular palp appears in zoea II; and pleopods appear in with a distal spine; endopod of the maxillula being 3- zoea III. It is interesting to note that although P. eremita has segmented in all stages; pleonal somites 2–5 with mediodorsal also 3 zoeal stages (Pike & Williamson, 1960), certain larval spines of different length (except for P. eremita); somite 5 with characters appear at an earlier stage in this species than in posterolateral spines; telson formula being usually 7 + 7, 8 + the rest of Paguristes having 3 zoeal stages. The rudiments 1 + 8 and 9 + 9 processes; uropods being nearly equal from of pleopods are already present in zoea I; the final numbers right to left, their endopod and exopod being fused to the pro- of telson processes (9 + 9) are attained in zoea II; and the topod in zoea III; small anal spine being present. In megalop, uropods are fully segmented on their emergence in zoea III the shared characters include: no ocular scales; cornea being (endopod and exopod being articulated to the protopod). narrower than the eyestalk; antennules and antennae being Unfortunately, the lack of larval information about most distinctly shorter than the chelipeds; antennular endopod Areopaguristes species does not allow us to provide the diag- being 2-segmented; chelipeds and uropods being nearly nosis of this genus and to summarize the larval characters dis- equal from right to left; telson being rounded, with numerous tinguishing Areopaguristes from Paguristes. The absence of long setae. any carapace spines and fused fourth telson process beyond Many authors believe that the anterolateral carapace spines zoea II are the possible zoeal characters diagnostic of the and posterolateral spines on the fifth pleonal somite are genus Areopaguristes. In the remaining larval characters, A. the characters diagnostic of Paguristes zoeas (Rice & nigroapiculus agree well with Paguristes species having 3 Provenzano, 1965; Provenzano, 1978; Quintana & Iwata, zoeal stages. The found differences between larvae of these 1987). It should be pointed out that zoea of A. nigroapiculus two genera lend support to the separation of Areopaguristes also has posterolateral spines on the fifth pleonal somite, but from Paguristes. lacks anterolateral carapace spines. Thus, the absence of any carapace spines can be treated as a possible larval character for Areopaguristes species. It is pertinent to note that ACKNOWLEDGEMENTS Diogenes larvae also possess both features mentioned above (Korn et al., 2008). Areopaguristes zoea shares many morpho- We are greatly indebted Dr Tomoyuki Komai (Natural logical features with the larvae not only of Paguristes but also History Museum and Institute, Chiba, Japan) for the identifi- of Diogenes and other diogenid genera. As noted by cation of Areopaguristes nigroapiculus females. This work was Provenzano (1968), only a combination of characters allows supported by the Russian Foundation for Fundamental distinguishing larvae of various diogenid genera from each Researches (grant number 08-04-00929). other. A very important character diagnostic to anomuran larvae is the armature of telson (McLaughlin et al., 1992, 1993). REFERENCES Based on the differences in the formation of the fourth telson process beyond the second zoeal stage, four informal Asakura A. (2006) Shallow water hermit crabs of the families groups of species are recognized in Diogenidae (Bartilotti Pylochelidae, Diogenidae and Paguridae (Crustacea: Decapoda: et al., 2008). Zoea of the genus Paguristes is referred to Anomura) from the Sea of Japan, with a description of a new group 4 where the telson processes are represented by setae species of Diogenes. Bulletin of the Toyama Science Museum 29, 23– in all the larval stages. Our data revealed that the fourth 103. telson process of A. nigroapiculus in zoea III is shorter than Bartilotti C., Calado R. and dos Santos A. (2008) Complete larval devel- that in the previous stage, fused to the telson, and lacks opment of the hermit crabs Clibanarius aequabilis and Clibanarius setules. 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McLaughlin P.A., Siddiqui F.A. and Crain J.A. (1993) Larval and early and juvenile development of Pagurus stevensae Hart, 1871 (Decapoda: Anomura: Paguridae) reared in the laboratory. Journal of Crustacean Thomson G.M. (1899) A revision of the Crustacea Anomura of New Biology 13, 322–342. Zealand. Transactions and Proceedings of the New Zealand Institute, Zoology 31, 169–197. McLaughlin P.A., Komai T., Lemaitre R. and Rahayu D.L. (2010) Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Correspondence should be addressed to: Galatheidae of the Galatheoidea). Part I—Lithodoidea, Lomisoidea E.S. Kornienko and Paguroidea. Rafﬂes Bulletin of Zoology Supplement 23, 5–107. A.V. Zhirmunsky Institute of Marine Biology Morgan G.J. (1987) Abbreviated development in Paguristes frontalis Far East Branch, Russian Academy of Sciences (Milne-Edwards, 1836) (Anomura: Diogenidae) from southern 17 Pal’chevskogo Street, 6900041, Vladivostok, Russia Australia. Journal of Crustacean Biology 7, 536–540. email: [email protected]