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Illustrated key for the identification of brachyuranmegalopae (Crustacea: Decapoda) in the plankton ofPeter the Great Bay (Sea of Japan)OLGA M. KORN a & ELENA S. KORNIENKO aa A.V. Zhirmunsky Institute of Marine Biology , Far East Branch, Russian Academy ofSciences, 17 Palchevskogo Street, 690041, Vladivostok, Russia Phone: +7 (4232) 310905Fax: +7 (4232) 310905 E-mail:Published online: 01 Dec 2010.
To cite this article: OLGA M. KORN & ELENA S. KORNIENKO (2010) Illustrated key for the identification of brachyuranmegalopae (Crustacea: Decapoda) in the plankton of Peter the Great Bay (Sea of Japan), Invertebrate Reproduction &Development, 54:3, 111-119, DOI: 10.1080/07924259.2010.9652323
To link to this article: http://dx.doi.org/10.1080/07924259.2010.9652323
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Invertebrate Reproduction and Development, 54:3 (2010) 111–119 111Balaban, Philadelphia/Rehovot
0168-8170/10/$05.00 © 2010 Balaban
Illustrated key for the identification of brachyuran megalopae(Crustacea: Decapoda) in the plankton of Peter the Great Bay
(Sea of Japan)
OLGA M. KORN and ELENA S. KORNIENKO*
A.V. Zhirmunsky Institute of Marine Biology, Far East Branch, Russian Academy of Sciences,17 Palchevskogo Street, 690041, Vladivostok, Russia
Tel. +7 (4232) 310905; Fax: +7 (4232) 310900; email: [email protected]
Received 26 March 2010; Accepted 9 June 2010
Abstract
A dichotomous key for brachyuran megalopae from Peter the Great Bay (Russian waters of the Sea
of Japan) is provided. The key covers 18 taxa identified to species level and uses only the external
characters of larvae that are easy to observe with a stereomicroscope without specimen dissection.
The key is mainly based on the new original descriptions of larvae obtained both from plankton
samples and from laboratory culture. Period of occurrence of larvae of each species in the plankton
is also presented.
Key words: Larvae, crab, northwestern Pacific, seasonal occurrence
Introduction
The megalopa is the last stage in brachyuran larval
development during which settlement to the juvenile
habitat occurs. In comparison with zoeal stages,
megalopae are not as well studied. These larvae are
rarely found in plankton samples, so their identification
presents considerable difficulties. To date, keys for the
identification of crab megalopae from the Northeastern
Atlantic (Ingle, 1992), Pacific Northwest (Puls, 2001),
and Mediterranean (Pessani et al., 2004) exist. Al-
though Konishi & Shikatani (2000) produced a key for
the identification of zoeal stages of commercially
important crabs in the coastal waters of Japan, only
remarks on the megalopae were given. Recently, we
published an illustrated key for the identification of
brachyuran zoea in Peter the Great Bay (northwestern
Sea of Japan) (Kornienko & Korn, 2009). The aim of
this work is to construct a key for identifying brachy-
uran megalopae in Russian waters of the Sea of Japan
and to document the seasonal occurrence of larvae in
the plankton.
Materials and Methods
Megalopae of most of the species included in the
key have been described (Table 1). However, our
identification key is mainly based on original material
taken from plankton samples and from larvae reared
from ovigerous females in the laboratory using a
method described earlier (Kornienko & Korn, 2007,
2009).
The seasonal occurrence of megalopae in the plank-
ton was studied using the materials of plankton surveys
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Table 1. List of species and sources of descriptions of brachyuran megalopae included in the identification key
Family Species Authors
Cancridae Latereille, 1802 Glebocarcinus amphioetus (Rathbun, 1898) Iwata & Konishi, 1981
Cheiragonidae Ortmann, 1893 Erimacrus isenbeckii (Brandt, 1848)Telmessus cheiragonus (Tilesius, 1812)
Kurata, 1963aKurata, 1963a
Dorippidae MacLeay, 1838 Paradorippe granulata (De Haan, 1841) Quintana, 1987
Epialtidae MacLeay, 1838 Pugettia quadridens (De Haan, 1839)
Pisoides bidentatus (A. Milne-Edwards,1873)
Kurata, 1969; Ko & Hwang, 1997;Kornienko & Korn, 2004Kornienko & Korn, 2007
Oregoniidae Garth, 1958 Chionoecetes opilio (O. Fabricius, 1788)
Hyas ursinus Rathbun, 1924
Kurata, 1963b; Makarov, 1966;Motoh, 1973Not described
Portunidae Rafinesque, 1815 Charybdis japonica A. Milne-Edwards,1861)
Yatsuzuka et al., 1984
Varunidae H. Milne Edwards,1853
Eriocheir japonica De Haan, 1835
Hemigrapsus sanguineus (De Haan, 1835)
H. penicillatus (De Haan, 1835)
H. longitarsis (Miers, 1839
Helice tridens (De Haan, 1835)
Morita, 1974; Lai et al., 1986; Kim& Hwang, 1990; Kornienko & Korn,2005aHwang et al., 1993; Kornienko et al.,2008Hwang & Kim, 1995; Kornienko etal., 2008Park & Ko, 2002; Kornienko et al.,2008Baba & Moriyama, 1972
Macrophtalmidae Dana, 1851 Tritodynamia rathbunae Shen, 1932 Matsuo, 1998
Pinnotheridae De Haan, 1833 Pinnixa rathbuni Sakai, 1934
Pinnaxodes mutuensis Sakai, 1939Sakaina yokoyai (Glassel, 1933)
Muraoka, 1979; Konishi, 1983;Kornienko & Korn, 2005bKonishi, 1981Kornienko & Korn, in press
performed in Amursky and Ussurijsky Bays (inner
bays of Peter the Great Bay, Sea of Japan), twice a
month, from April to October 2007 and 2008 (Fig. 1).
Zooplankton samples were taken at 66 stations, at a
depth ranging from 2 to 75 m, across the entire water
column, from bottom to surface. A Juday net with a
ring diameter of 38 cm and a filtering cone made of a
168 mm mesh was used. Simultaneously, the tempera-
ture was measured at the water surface. In addition,
numerous qualitative plankton samples were collected
in Vostok Bay (inner bay of Peter the Great Bay), at a
depth of 3 m, at night using a light source. Decapod
larvae have a positive phototaxis, hence this method is
effective for the study of their species diversity.
All megalopae were fixed in 4% formaldehyde for
light microscopic studies. The carapace length from the
top of rostrum to the posterior midpoint (CL) and the
maximal carapace width without spines (CW) are
represented in Table 2. At least 10 larvae of each
species were examined and measured. Exceptions were
the megalopae of Hyas ursinus and Pinnaxodes mutu-
ensis, for which we found only one specimen of each
species. The outlines of the larvae were drawn using a
camera lucida attached to a binocular Ergaval
microscope (Carl Zeiss Jena). The main characters of
brachyuran megalopae used for identification are
shown in Fig. 2.
For the identification key we tried to use only the
external characters of larvae that are easy to observe
using a stereomicroscope without specimen dissection.
In a previous paper devoted to the description of
zoeal stages (Kornienko & Korn, 2009), the taxonomic
position of brachyuran species was represented
according to Martin & Davis (2001). In this study we
used the new catalogs of Brachyura (Ng et al., 2008;
De Grave et al., 2009). These monographs insert some
amendments in taxonomy of this group which are
confirmed by the larval morphology.
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Fig. 1. Map showing the sampling area.
Table 2. Measurements of brachyuran megalopae (meanvalues ± standard deviation, µm) from the plankton of Peterthe Great Bay
Species Carapacelength
Carapacewidth
Glebocarcinus amphioetus 2.27±0.11 1.42±0.08Erimacrus isenbeckiiTelmessus cheiragonus
4.40±0.202.96±0.10
3.19±0.501.92±0.31
Paradorippe granulata(after Quintana, 1987)
2.94 2.68
Pugettia quadridens* 1.26±0.20 1.09±0.20Pisoides bidentatus 1.34±0.08 0.91±0.05Chionoecetes opilioHyas ursinus
2.96±0.162.64
2.13±0.141.49
Charybdis japonica(after Yatsuzuka et al., 1984)
2.10 0.80
Eriocheir japonica*Hemigrapsus sanguineus*H. penicillatus*H. longitarsis*Helice tridens
1.87±0.071.78±0.151.58±0.141.52±0.141.95±0.07
1.70±0.171.63±0.141.44±0.071.43±0.101.40±0.03
Tritodynamia rathbunae 2.43±0.19 2.15±0.26Pinnixa rathbuniPinnaxodes mutuensisSakaina yokoyai
1.53±0.070.951.64±0.06
1.99±0.140.951.43±0.08
*Sizes of larvae from laboratory culture.
Fig. 2. Main characters used for the identification of brachy-uran megalopae. A, dorsal view of megalopa; B, maxilliped;C, pleopod; D, pereopod.
Results
Key for the identification of brachyuran megalopaein the plankton of Peter the Great Bay
1a. Carapace with spines (Fig. 3A–D). . . . . . . . . . . 2
1b. Carapace without spines (Fig. 3E, F). . . . . . . . 10
2a. Carapace with dorsolateral spines (Fig. 3À, B). 3
2b. Carapace without dorsolateral spines. . . . . . . . . 4
3a. Carapace with one posterodorsal spine (Fig. 3A)
.. . . . . . . . . . . . . . . . . . . . . . . . Hyas ursinus (Fig. 9A)
.. . . . . . . . . . . . . . . . . . . . . [Megalopa found in June]
3b. Carapace with two posterodorsal spines (Fig. 3B)
.. . . . . . . . . . . . . . . . . . . Chionoecetes opilio (Fig. 9B)
.. . . . . . . . . . . . . [Megalopae found in May and June]
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Fig. 3. Carapace of megalopa in Hyas ursinus (A), Chio-noecetes opilio (B), Paradorippe granulata (after Quintana,1987) (C), Pinnixa rathbuni (D), Eriocheir japonica (E),Pinnaxodes mutuensis (F), dorsal view.
Fig. 4. Antenna of megalopa in Tritodynamia rathbunae (A)and Glebocarcinus amphioetus (B).
4a. Carapace with one posterodorsal spine. . . . . . . 5
4b. Carapace without posterodorsal spines. . . . . . . 6
5a. Rostrum curved ventrally; long setae on three distal
antennal segments form a dense bunch (Fig. 4A)
.. . . . . . . . . . . . . . . Tritodynamia rathbunae (Fig. 9C)
[Megalopae found from July to September]
5b. Rostrum directed forward; short and sparse
antennal setae do not form a bunch (Fig. 4B)
Fig. 5. Distal segments of pereopods IV and V of megalopain Paradorippe granulata (after Quintana, 1987) (A, B),pereopod V in Charybdis japonica (after Yatsuzuka et al.,1984) (C), Sakaina yokoyai (D), and Pisoides bidentatus (E).
Fig. 6. Abdomen of megalopa in Telmessus cheiragonus (A)and Erimacrus isenbeckii (B).
.. . . . . . . . . . . . . Glebocarcinus amphioetus (Fig. 9D)
.. . . . . . . . . . [Megalopae found from July to October]
6a. Carapace width greater than length; eye stalks very
short (fig. 3D)
.. . . . . . . . . . . . . . . . . . . . . Pinnixa rathbuni (Fig. 9E)
.. . . . . . . [Megalopae found from June to November]
6b. Carapace width less than length; eye stalks of usual
length. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
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Fig. 7. Carapace of megalopa in Pisoides bidentatus (A) andPugettia quadridens (B), lateral view.
7a. Pereopods IV and V distinctly subchelate(Fig. 5À, B)
.. . . . . . . . . . . . . . . . Paradorippe granulata (Fig. 9F)
.. . . . . . . . . . . . . . . . . . . . . . . . [Megalopae not found]
7b. Pereopods IV and V not subchelate. . . . . . . . . . 8
8a. Carapace pear-shaped; dactylus of pereopod V with
three long terminal setae (Fig. 5D)
.. . . . . . . . . . . . . . . . . . . . . Sakaina yokoyai (Fig. 9G)
.. . . . . . . . [Megalopae found from July to September]
8b. Carapace nearly rectangular; dactylus of pereopod
V without long terminal setae (Fig. 5E). . . . . . . . . . 9
9a. Posterior ventrolateral projections on the abdominal
somite 5 longer than somite 6 (Fig. 6A)
.. . . . . . . . . . . . . . . . Telmessus cheiragonus (Fig. 9H)
.. . . . . . . . . . . . . [Megalopae found in May and June]
9b. Posterior ventrolateral projections on the abdo-
minal somite 5 shorter than somite 6 (Fig. 6B)
.. . . . . . . . . . . . . . . . . . . Erimacrus isenbeckii (Fig. 9I)
.. . . . . . . . . . . . . [Megalopae found in May and June]
10a. Dactylus of pereopod V with long terminal setae
.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
10b. Dactylus of pereopod V without long terminal
setae. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
11a. Dactylus of pereopod V paddlelike, with four long
terminal setae (Fig. 5C); sternum of pereopod IV with
long sharp spine turned backwards
.. . . . . . . . . . . . . . . . . . . Charybdis japonica (Fig. 9J)
.. . . . . . . . . . . . . . . . . . . . . . . . [Megalopae not found]
Fig. 8. Last abdominal segments and telson of megalopa inEriocheir japonica (A), Helice tridens (B), and Hemigrapsussanguineus (C).
11b. Dactylus of pereopod V not paddlelike, with three
long terminal setae; spine on the sternum of pereopod
IV inconspicuous. . . . . . . . . . . . . . . . . . . . . . . . . . 14
12a. Carapace width equal carapace length
.. . . . . . . . . . . . . . . . . Pinnaxodes mutuensis (Fig. 9K)
.. . . . . . . . . . . . . . . . . . . . . . [Megalopa found in July]
12b. Carapace width less than carapace length. . . 13
13a. Central tubercle on the carapace surface high
(Fig. 7À)
.. . . . . . . . . . . . . . . . . . . Pisoides bidentatus (Fig. 9L)
.. . . . . . . . . . [Megalopae found from July to October]
13b. Central tubercle on the carapace surface low(Fig. 7B)
.. . . . . . . . . . . . . . . . . . Pugettia quadridens (Fig. 9M)
.. . . . . . . . . . [Megalopae found from July to October]
14a. Posterior ventrolateral projections on the abdo-
minal somite 5 longer than somite 6 (Fig. 8À); basal
segment of pleopod V with two plumose setae
.. . . . . . . . . . . . . . . . . . . Eriocheir japonica (Fig. 9N)
.. . . . . . . . [Megalopae found from July to September]
14b. Posterior ventrolateral projections on the abdo-
minal somite 5 equal or shorter than somite 6; basal
segment of pleopod V with one plumose seta. . . . 15
15a. Posterior ventrolateral projections on the abdo-
minal somite 5 equal somite 6 (Fig. 8B)
.. . . . . . . . . . . . . . . . . . . . . . . Helice tridens (Fig. 9O)
.. . . . . . . . . . . . . . . . . . . . . [Megalopae found in May]
15b. Posterior ventrolateral projections on the abdo-
minal somite 5 shorter than somite 6 (Fig. 8C). . . 16
16a. Antennular exopod 5-segmented
.. . . . . . . . . . . . . . . . . . . . . . Hemigrapsus penicillatus
.. . . . . . . . [Megalopae found from July to September]
16b. Antennular exopod 4-segmented. . . . . . . . . . 17
17a. Third antennular segment with 9 aesthetascs
.. . . . . . . . . . . . . . . Hemigrapsus sanguineus (Fig. 9P)
.. . . . . . . . [Megalopae found from July to September]
17b. Third antennular segment with 7 aesthetascs
.. . . . . . . . . . . . . . . . . . . . . . . Hemigrapsus longitarsis
.. . . . . . . . [Megalopae found from July to September]
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Fig. 9. Dorsal view of megalopa in Hyas ursinus (A), Chionoecetes opilio (B), Tritodynamia rathbunae (C), Glebocarcinusamphioetus (D), Pinnixa rathbuni (E), Paradorippe granulata (after Quintana, 1987) (F), Sakaina yokoyai (G), Telmessuscheiragonus (H), Erimacrus isenbeckii (I), Charybdis japonica (after Yatsuzuka et al., 1984) (J), Pinnaxodes mutuensis (K),Pisoides bidentatus (L), Pugettia quadridens (M), Eriocheir japonica (N), Helice tridens (O), and Hemigrapsus sanguineus(P).
Seasonal occurrence of larvae in the plankton ofPeter the Great Bay
Brachyuran megalopae were rarely encountered in
the plankton of Peter the Great Bay. They were found
throughout the entire water area, over depths of 2–
75 m, with maximal density of 1–2 specimens/m . The3
larvae occurred from late May to early November, at a
water temperature ranging from 7 to 23ºC (Table 3).
Discussion
In Peter the Great Bay, brachyuran megalopae
of only 16 species have been found during our inves-
tigation. Megalopae of Charybdis japonica and Para-
dorippe granulata were not encountered in our
material and their descriptions are from Yatsuzuka et
al. (1984) and Quintana (1987). While brachyuran
zoeal stages were abundant throughout the entire water
area, attaining several hundred specimens/m , mega-3
lopal stages were only sporadic, being numerous in
qualitative night samples. These larvae were used for
drawings and dimensions.
Megalopae of large commercial species, Chiono-ecetes opilio, Erimacrus isenbeckii and Telmessuscheiragonus, were found in spring, at low tempera-tures. The larvae of the rest small brachyuran specieswere usually encountered in summer and autumn, athigher temperatures. The pea crab, Pinnixa rathbuni,possessed the most prolonged pelagic period, mega-lopae of this species were found in the plankton duringthe six months — between June and November.
The greatest difficulties are connected with theidentification of varunid larvae in the plankton of Peterthe Great Bay. Kornienko et al. (2008) have shown thatthe zoea of three Hemigrapsus species are first dis-tinguishable at stage III only, whereas the larvae ofEriocheir japonica possess a number of distinctivefeatures at all zoeal stages. In the case of megalopae,all four species are very similar and differ mainly in thelength of the posterior ventrolateral projections on theabdominal somite 5 (Fig. 8). Zoea and megalopae ofHelice tridens were found in the plankton of thisregion only recently. These larvae are also very similarto the larvae of the previous two genera, but are easierrecognized because they occur in the plankton in
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Table 3. Seasonal occurrence of brachyuran megalopae in the plankton of Peter the Great Bay (Sea of Japan)
Species Months
March April May June July August September October November
Glebocarcinus amphioetus + + + +Erimacrus isenbeckii + +Telmessus cheiragonus + +Paradorippe granulata Not foundPugettia quadridens + + + +Pisoides bidentatus + + + +Chionoecetes opilio + +Hyas ursinus +Charybdis japonica Not foundEriocheir japonica + + +Hemigrapsus sanguineus + + +H. penicillatus + + +H. longitarsis + + +Helice tridens +Tritodynamia rathbunae + + +Pinnixa rathbuni + + + + + +Pinnaxodes mutuensis +Sakaina yokoyai + + +
spring, whereas the larvae of E. japonica and Hemi-
grapsus species are found only in summer.Kornienko & Korn (2007) have shown that zoeal
stages of two spider crabs, Pugettia quadridens and
Pisoides bidentatus, inhabiting Russian waters of the
Sea of Japan are nearly identical. However, the mega-
lopae of these species differ, the central tubercle on the
carapace is more elevated in P. bidentatus than in P.
quadridens.
In Peter the Great Bay, the lyre crab Hyas ursinus
occurs more rarely, compared to other brachyuran
species, and its larvae have not been described yet. We
have not found zoeal stages of this species (Kornienko
& Korn, 2009); however, we found a single megalopa
belonging to the genus Hyas. This larva differs greatly
from megalopa of another oregoniid species Chiono-
ecetes opilio in having one (not two) posterodorsal
carapace spine.
Chionoecetes opilio is closely related to its con-
generic species C. japonicus, which is common in the
coastal waters of Japan. The identification of the larvae
of two snow crabs is very difficult. The zoea and
megalopae of both species are very similar, and there
are discrepancies in the descriptions (see Kurata,
1963b; Motoh, 1973, 1976; Haynes, 1981) of their
distinctive characters. The possibility of natural inter-
breeding between C. opilio and C. japonicus has also
been reported (Nishimura & Mizusawa, 1969). In most
plankton studies, the larvae of both species are not
distinguished from each other and named Chionoecetes
spp. (Fukataki, 1969; Ito & Ikehara, 1971; Kon et al.,2003). Since C. japonicus inhabits greater depths (up
to 2700 m) than C. opilio (up to 400 m), we believe
that the larvae only of C. opilio have been found in
Peter the Great Bay.
Acknowlegements
We are greatly indebted to A.S. Sokolovsky, L.C.
Shkoldina and I.V. Epur (A.V. Zhirmunsky Institute of
Marine Biology, FEB RAS) for kindly loaned plankton
samples from Peter the Great Bay. The project was
supported by the Russian Foundation for Fundamental
Researches (grant no. 08-04-00929).
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