Journal of the Marine
Biological Association of the
United Kingdom
cambridge.org/mbi
Morphological observations and molecular
confirmation of larvae of Levisquilla inermis
(Crustacea: Stomatopoda) from the Seto Inland
Sea
Alyaa Elsaid Abdelaziz Fadl1,2
Original Article
Cite this article: Fadl AEA, Yamaguchi S,
Wakabayashi K (2021). Morphological
observations and molecular confirmation of
larvae of Levisquilla inermis (Crustacea:
Stomatopoda) from the Seto Inland Sea.
Journal of the Marine Biological Association of
the United Kingdom 101, 801–810. https://
doi.org/10.1017/S002531542100076X
Received: 15 June 2021
Revised: 19 October 2021
Accepted: 21 October 2021
First published online: 24 November 2021
Key words:
16S rRNA; cincinnuli; crustaceans; DNA
barcoding; mantis shrimp; stomatopod larvae;
taxonomy
Author for correspondence:
Kaori Wakabayashi,
E-mail: kaoriw@hiroshima-u.ac.jp
, Shuhei Yamaguchi3 and Kaori Wakabayashi1
1
Graduate School of Integrated Sciences for Life, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima,
Hiroshima 739–8528, Japan; 2Department of Zoology, Faculty of Science, Kafrelsheikh University, Kafr Elsheikh,
Egypt and 3School of Applied Biological Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima,
Hiroshima 739–8528, Japan
Abstract
Mantis shrimps are commercially important crustaceans in many areas of the world. In contrast to the relatively common studies of adults, limited studies have been attempted of larvae
because of a lack of identification keys. The objectives of this study were two-fold: (1) to link
wild-caught larval specimens from the Seto Inland Sea to a certain species and (2) to present a
detailed morphological description of the last larval stage. The resulting molecular phylogenetic tree based on 16S rRNA gene sequences strongly implies that our larval specimens were
linked to Levisquilla inermis, which was barcoded from a newly collected adult specimen with
a morphological identification. K2P genetic divergence was found to be 0% among the larval
and adult specimens. The congeneric species L. jurichi was the sister group of the L. inermis
cluster, but the K2P distance between them was 3.4%, and it was considered a distinct species.
Morphological observations provided five major distinguishing characteristics of the last-stage
larva of L. inermis: (1) propodus of second maxilliped with three basal spines, (2) all five pleopods possessing an appendix interna with cincinnuli, (3) exopod of uropod longer than the
endopod, (4) distal margin of the exopod of the uropod reaching the lateral tooth of telson,
and (5) telson with nine intermediate denticles. Overall, our results reveal the importance of
combining molecular and morphological analyses for solving stomatopod larval identification.
This finding can be used to support and facilitate future research on the taxonomy and biodiversity of stomatopod larvae.
Introduction
© The Author(s), 2021. Published by
Cambridge University Press on behalf of
Marine Biological Association of the United
Kingdom
Mantis shrimps or stomatopods (Crustacea: Malacostraca) are predatory marine crustaceans,
which are found mainly in tropical and subtropical coastal waters and are characterized by
the remarkably developed second maxilliped that has been modified as a powerful raptorial
appendage (Ahyong et al., 2008). Almost 500 species of stomatopods are known and divided
into 17 families within seven superfamilies (Ahyong & Harling, 2000; Ahyong et al., 2008; Van
Der Wal & Ahyong, 2017; Hwang et al., 2019; WoRMS, 2021). The life history of stomatopods
involves a series of larval stages consisting of short propelagic and long pelagic phases. The
last-stage larval metamorphosizes into a post-larva and settles into the adult benthic habitat
after a single moult (Pyrne, 1972; Feller et al., 2013). Larval forms of stomatopods are highly
specialized among crustacean larvae as they possess a remarkable set of morphological characteristics such as large, fully functional raptorial second maxillipeds and often large body size
that can be up to 50 mm in total length (Ahyong et al., 2014; Wiethase et al., 2020).
Stomatopods can exhibit a greater variety of ecological adaptations in larvae than in adults
due to their distinct larval forms (Haug et al., 2016).
While all stages of the stomatopod larvae can be clearly recognized from other crustacean
larvae, identifying them to the species level based on their morphological characters is still difficult. Only around 10% of known species could be identified in their larval stages (Diaz, 1998;
Haug et al., 2016). Traditionally, the identification of stomatopod larvae has been performed
either by hatching larvae from a known adult or by cultivating wild-caught larvae to adulthood; however, these laboratory methods are time-consuming and extremely challenging
(Provenzano & Manning, 1978; Diaz, 1998; Feller et al., 2013). Descriptions of the entire series
of larval stages using those two methods exist for five of the 500 extant species: (1)
Neogonodactylus oerstedii (Hansen, 1895) (as Gonodactylus oerstedii) (Manning &
Provenzano, 1963; Provenzano & Manning, 1978), (2) Neogonodactylus wennerae Manning
& Heard, 1997 (as Gonodactylus bredini Manning, 1969) (Morgan & Goy, 1987), (3)
Pterygosquilla schizodontia (Richardson, 1953) (as Squilla armata H. Milne Edwards, 1837)
(Pyne, 1972), (4) Heterosquilla tricarinata (Claus, 1871) (Greenwood & Williams, 1984)
and (5) Oratosquilla oratoria (De Haan, 1833–1850) (Hamano & Matsuura, 1987). Even partial larval series are known only for a restricted number of species (Gurney, 1946; Alikunhi,
1967; Michel, 1968, 1970; Michel & Manning, 1972; Shanbhogue, 1975; Rodrigues &
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Manning, 1992; Ahyong, 2002; Veena & Kaladharan, 2010; Feller
et al., 2013; Cházaro-Olvera et al., 2018). Therefore, a scarcity of
information linking larvae to adult forms clearly exists. To overcome the obstacles and complexities of traditional taxonomic
methods, particularly for groups of species with multiple developmental stages, DNA barcoding as a taxonomic method has been
applied for the early life stages (Abinawanto et al., 2019).
DNA barcoding, proposed by Hebert et al. (2003), is one of the
molecular identification methods that is intensely applied in taxonomic study of groups and an effective tool for linking larvae with
their adults. DNA barcoding was originally performed by analysing the short nucleotide sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene from taxonomically
unidentified specimens and comparing them with the known
sequences stored in public databases, such as the GenBank database and Barcode of Life database. Nowadays, diverse gene regions
are successfully used for DNA barcoding in a wide range of both
aquatic and terrestrial animal taxa (Hebert et al., 2004a, 2004b;
Hajibabaei et al., 2006; Wakabayashi et al., 2006, 2017; Hubert
et al., 2008; De Grave et al., 2015; Carreton et al., 2019). A
DNA barcode is also useful to identify larvae collected from the
field into species by matching with the available sequences from
GenBank. Such methods have already been applied to crabs, barnacle larvae, fish larvae and stomatopods (Tang et al., 2010; Chen
et al., 2013; Chu et al., 2019; Li et al., 2019; Wei et al., 2021; Wong
et al., 2021). In addition, DNA barcoding as a method for identifying stomatopod larvae has been used not only for taxonomy
(Barber & Erdmann, 2000; Feller et al., 2013) but also for experimental (Feller & Cronin, 2014; Feller et al., 2019) and diversity or
distribution studies (Barber et al., 2002; Barber & Boyce, 2006;
Tang et al., 2010; Abinawanto et al., 2019). Although this method
has been utilized effectively for stomatopod identification, it is still
in the early stages of development since the DNA sequences available for barcoding stomatopods (such as COI and 16S rRNA
genes) are limited (Tang et al., 2010). Therefore, as demonstrated
in the current study, the assignment of larval specimens to the
species level may need the addition of more sequences from the
adult specimens with verified morphological identification.
Although the diagnostic morphologies of stomatopod larvae
are scarce, the late-stage larvae are easily classified into at least
the superfamily level using the morphological characters of carapace, abdomen, uropods and telson (Ahyong et al., 2014). The
larvae of the superfamily Squilloidea can be distinguished from
those of the other superfamilies based on a flatter carapace and
a slender abdomen (Ahyong et al., 2014). In Japan, 25 out of
70 recorded species are classified in the Squilloidea (Ahyong,
2012; Osawa & Fujita, 2016; Nakajima et al., 2020) and among
them, late-stage larvae have been described in 12 squilloid species
(Alikunhi, 1944, 1952, 1975; Manning, 1962; Hamano &
Matsuura, 1987; Zheng et al., 2006; Veena & Kaladharan, 2010;
Wong et al., 2021). During our recent cruise in the Seto Inland
Sea of Japan, late-stage larvae with a pair of large orange spots
on the basal part of the fifth pleopods were found. Such larvae
have not been described until now. In this paper, we document
a detailed morphological description of the squilloid larvae,
which were confirmed as Levisquilla inermis (Manning, 1965)
via a DNA barcoding technique using an adult specimen found
at the same location on the same day.
Materials and methods
Sampling
The larval specimens were sorted from plankton samples collected by an Ocean Research Institute (ORI) net (Omori, 1965;
Omori et al., 1965) with a diameter of 160 cm and mesh size of
Alyaa Elsaid Abdelaziz Fadl et al.
Fig. 1. Levisquilla inermis (Manning, 1965), live: (A) larva (ventral); (B) adult (dorsal).
Scale bars: A, 1 mm; B, 5 mm.
0.33 mm that was operated by the crew of the training and
research vessel ‘TOYOSHIO MARU’, Hiroshima University. The
net was towed in the Seto Inland Sea (33°49′ 59′′ N 132°23′ 41′′ E)
at a depth of 30–40 m on 29 October 2020. The adult specimen
was found in sediment that was dredged from a depth of 70 m
at the same location on the same day. Both live larval and adult
specimens were photographed (Figure 1) and then preserved in
99% ethanol for subsequent morphological and molecular
analyses.
Morphological observation
The larval specimens were observed and dissected under a stereomicroscope (SZX-9, Olympus). The stereomicroscope was also
used for morphometric characteristics, including the total length
(TL) from the tip of the rostrum to the apex of the submedian
tooth on the telson, the rostrum length (RL) from the tip to the
base of the rostrum, the carapace length (CL) as the distance
from the base of the anterolateral spine to the base of the posterolateral spine on the carapace, and the carapace width (CW) as
the maximum distance across the carapace. The dissected appendages were preserved in 70% ethanol or mounted on glass slides
using a mounting agent (CMCP-10 high-viscosity mountant;
Polysciences, Warrington, PA, USA), and then observed under
a compound microscope (BX-51, Olympus). The developmental
stage of the larval specimens was determined according to
Hamano & Matsuura (1987). They hatched larvae from females
of the Japanese mantis shrimp and illustrated the entire sequence
of larval stages in detail.
Illustrations for larval and adult specimens were created with
the aid of the camera lucida attachment (U-DA, Olympus). The
terminology of the body structure followed the structures of
Hamano & Mantsuura (1987), Ahyong (2001) and Feller et al.
(2013).
An adult male mantis shrimp was also included for the gene
analysis to confirm larval identity. This specimen was morphologically identified as Levisquilla inermis based on the dactylus
claw with six teeth (Figure 2A), the fifth thoracic somite with
short, anteriorly recurved spine (Figure 2B), the absence of supplementary carinae on the dorsolateral surface of the telson
(Figure 2C), and the absence of a post-anal carina. The total
length measured from the tip of the rostral plate to the apices
of the submedian teeth of the telson was 25.4 mm, and carapace
length measured along the dorsal midline excluding the rostral
plate was 6.1 mm.
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Journal of the Marine Biological Association of the United Kingdom
Fig. 2. Levisquilla inermis (Manning, 1965), adult male: (A) right raptorial claw (lateral); (B) lateral processes of fifth, sixth and seventh thoracic somites; (C) last abdominal somite and telson (dorsal). Scale bars: A–C, 1 mm.
Both larval (NSMT-Cr 29221, 29222) and adult (NSMT-Cr
29223) specimens were deposited in the crustacean collections
of the National Museum of Nature and Science, Tsukuba, Japan
(NSMT).
Molecular analysis
Genomic DNA was extracted from one pleopod with some pleon
muscles of both larval and adult specimens using NucleoSpin®
Tissue XS (Cat. no. 740901.50, Machery-Nagel, Germany) according to the manufacturer’s instructions. A polymerase chain reaction (PCR) was used to amplify the partial sequence of the
mitochondrial large subunit ribosomal RNA (16S rRNA) gene
in 50 μl of reaction volume using the following primers: (1)
1471 and (2) 1472 (Crandall & Fitzpatrick, 1996).
The PCR reaction mixture contained 50–100 ng DNA template, 0.2 μM of each primer, 5 μl of 10 × polymerase buffer, 0.2
mM of dNTPs and 1.25 unit of Taq polymerase. PCR was performed using a thermal cycler (Thermal Cycler Dice ® Touch,
TaKaRa, Japan) under the following temperature conditions: (1)
initial denaturation at 94 °C for 5 min, (2) followed by 35 cycles
of denaturation at 94 °C for 30 s, (3) annealing at 50 °C for 30 s,
(4) extension at 72 °C for 1 min and (5) a final extension at
72 °C for 10 min. The PCR products were visualized on a 1.5%
agarose gel to confirm the size and quality and then purified
using the Qiaquick Gel Extraction Kit (Qiagen, Germany).
Cycle sequencing for the PCR products was performed using
BigDye™ Terminator v3.1 Cycle Sequencing Kit (Applied
Biosystems, USA) under the following temperature regimes: (1)
denaturation at 96 °C for 30 s, (2) annealing at 50 °C for 15 s,
and (3) extension at 60 °C for 4 min. These steps were repeated
for 25 cycles. Nucleotide sequences of the amplified fragments
were post-purified and then evaluated with capillary electrophoresis using an ABI PRISM 3130 xl Genetic Analyzer (Applied
Biosystems) at the Natural Science Center for Basic Research
and Development, Hiroshima University. All sequences were
checked on the Sequence Scanner Software v2.0 (Applied
Biosystems). Bases expressing ‘N’ were visually checked with the
original waveforms. The nucleotide sequences of the studied species were deposited under OK575769–OK575771 through the
International Nucleotide Sequence Database Collaboration at
the National Center for Biotechnology Information, Bethesda,
MD, USA.
Multiple sequence alignment was performed using MUSCLE
(Edgar, 2004) on MEGA 7 (Kumar et al., 2016). Gblocks
v.0.91b (Castresana, 2000) was used to eliminate divergent regions
and inadequately aligned positions in the dataset; 306 positions in
total were used in the final dataset. Neighbour-joining (NJ) tree
with bootstrap analysis (10,000 replications) was constructed
based on the Kimura 2-parameter (K2P) model (Kimura, 1980)
using MEGA 7. The 16S rRNA gene sequences resulting from
the 44 squilloid species are currently available from the
GenBank, and 42 species among them were acquired for the
molecular analysis (Belosquilla laevis [KR153534] formed a long
branch, Cloridina moluccensis [MH168209] completely matched
with Busquilla quadraticauda [MH168223]) as shown in
Table 1. Up to three sequences were selected to represent a species
when several different sequences were available within a species
(applied to 12 species in total) in which those sequences derived
from the different studies were clustered for all 12 species; thus,
the terminal branch of each species was compressed in the final
tree (Figure 3, Supplementary Figure S1). Three species from
the superfamily Parasquilloidea were selected as the outgroups
because of their close relationship to Squilloidea (Van Der Wal
et al., 2017, 2019). The analysis involved 67 nucleotide sequences
from 46 species of mantis shrimp.
Results
Molecular identification of stomatopod larvae
The K2P genetic distances of the 16S rRNA gene were 1% or below
within species (Supplementary Table S1) except for the distances in
Alima orientalis and Oratosquilla oratoria (3.7% and 0.3–1.3%,
respectively) in which the greater sequence divergences were indicated (Du et al., 2016; Cheng & Sha, 2017; Wong et al., 2021).
The constructed phylogenetic tree (Figure 3) placed the two
larval individuals with the adult sequence of Levisquilla inermis.
The sequences from the two larval individuals were identical,
and only one out of 306 base positions was different from the
adult L. inermis specimen. The K2P genetic distance was below
0.1% among the three sequences. The larval and adult L. inermis
shared the most common ancestor with Levisquilla jurichi
(Makarov, 1979) with the K2P genetic distance of 3.4%.
Taxonomic account
SYSTEMATICS
Order STOMATOPODA Latreille, 1817
Suborder UNIPELTATA Latreille, 1825
Superfamily SQUILLOIDEA Latreille, 1802
Family SQUILLIDAE Latreille, 1802
Genus Levisquilla Manning, 1977
Levisquilla inermis (Manning, 1965)
(Japanese name: Subesube-shako)
(Figures 1, 4, 5)
Material examined. Last larval stage, NSMT Cr-29221, 15.95
mm in TL, Seto Inland Sea, Japan, 30–40 m, 29 October 2020.
Description
Carapace (Figure 4A–C). Elongated; 3.83 mm in CL, 1.90 mm in
CW, 3.30 mm in RL, ventral armed with 6 spinules; armed with 2
anterolateral spines extending to the base of the eyestalk, 2 posterolateral spines extending to the second pleomere, and 1 median
spine on posterior margin. Posterior margin of carapace reaching
thoracic somite 7.
Antennule (Figure 4D). Antennular stalk 3-segmented. First
stalk segment with 4 setae, the second segment with 6 setae,
and the third segment with 1 seta. Antennule with 3 setaceous
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Table 1. Stomatopod species and the sequence references of 16S rRNA gene used in this study
Species
Accession Nos.
References
Squilloidea
Squillidae
Alima maxima
MH168208
Van Der Wal et al. (2019)
Alima orientalis
HM138813
Porter et al. (2010)
MH168229
Van Der Wal et al. (2019)
Alima pacifica
HM138814
Porter et al. (2010)
Anchisquilla fasciata
FJ224251
Tang et al. (2010)
FJ224252
Tang et al. (2010)
MH168211
Van Der Wal et al. (2019)
Busquilla plantei
HM138815
Porter et al. (2010)
Busquilla quadraticauda
MH168223
Van Der Wal et al. (2019)
Carinosquilla multicarinata
MH168221
Van Der Wal et al. (2019)
Clorida decorata
MH168200
Van Der Wal et al. (2019)
FJ224253
Tang et al. (2010)
Cloridopsis scorpio
MH168234
Van Der Wal et al. (2019)
Dictyosquilla foveolata
FJ224256
Tang et al. (2010)
MW864094
Zhou (2021)a
MH168236
Van Der Wal et al. (2019)
Erugosquilla graham
MH168226
Van Der Wal et al. (2019)
Erugosquilla woodmasoni
FJ224262
Tang et al. (2010)
KU532327
Du et al. (2016)
MH168225
Van Der Wal et al. (2019)
Fallosquilla fallax
HM138821
Porter et al. (2010)
Harpiosquilla annandalei
MH168202
Van Der Wal et al. (2019)
Harpiosquilla harpax
AY699271
Miller & Austin (2006)
MH168203
Van Der Wal et al. (2019)
FJ224264
Tang et al. (2010)
Harpiosquilla melanoura
MH168201
Van Der Wal et al. (2019)
Kempella mikado
MH168199
Van Der Wal et al. (2019)
FJ871138
Tang et al. (2010)
HM138833
Porter et al. (2010)
Kempella stridulans
MH168213
Van Der Wal et al. (2019)
Lenisquilla lata
MH168235
Van Der Wal et al. (2019)
Levisquilla intermis
OK575769
This study
(larva, NSMT-Cr 29221)
OK575771
This study
(larva, NSMT-Cr 29222)
OK575770
This study
Levisquilla jurichi
MH168204
Van Der Wal et al. (2019)
Leptosquilla schmeltzii
MH168222
Van Der Wal et al. (2019)
Lophosquilla costata
MH168237
Van Der Wal et al. (2019)
MT276143
Zhang et al. (2020)
Meiosquilla dawsoni
MH168206
Van Der Wal et al. (2019)
Meiosquilla swetti
MH168210
Van Der Wal et al. (2019)
Miyakea nepa
FJ224268
Tang et al. (2010)
MH168205
Van Der Wal et al. (2019)
Miyakea holoschista
MH168230
Van Der Wal et al. (2019)
Oratosquilla fabricii
MH168227
Van Der Wal et al. (2019)
(Continued )
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Table 1. (Continued.)
Species
Accession Nos.
References
KU532325
Du et al. (2016)
MH168214
Van Der Wal et al. (2019)
FJ224273
Tang et al. (2010)
GQ292769
Liu & Cui (2010)
Oratosquillina anomala
MH168217
Van Der Wal et al. (2019)
Oratosquillina asiatica
MH168238
Van Der Wal et al. (2019)
Oratosquillina inornata
MH168220
Van Der Wal et al. (2019)
Oratosquillina interrupta
MH168219
Van Der Wal et al. (2019)
Oratosquillina perpensa
MH168218
Van Der Wal et al. (2019)
Pterygosquilla schizodontia
MH168216
Van Der Wal et al. (2019)
Quollastria imperialis
MH168207
Van Der Wal et al. (2019)
Rissoides barnardi
MH168228
Van Der Wal et al. (2019)
Squilla empusa
DQ191684
Swinstrom et al. (2005)
Squilla mantis
GQ328956
Koenemann et al. (2010)
AY639936
Cook et al. (2005)
Oratosquilla oratoria
Squilla rugosa
HM138854
Porter et al. (2010)
Squilloides leptosquilla
KR095170
Kang et al. (2015)a
MH168224
Van Der Wal et al. (2019)
Vossquilla kempi
MH168212
Van Der Wal et al. (2019)
Triasquilla profunda
MH168215
Van Der Wal et al. (2019)
Faughnia haani
MW632159
Hwang (2021)a
Faughnia serenei
MH168232
Van Der Wal et al. (2019)
Pseudosquillopsis marmorata
HM138845
Porter et al. (2010)
Parasquilloidea
Parasquillidae
a
Direct submission to GenBank.
flagella. Inner flagellum 9-segmented with 1 long seta on the first
segment, many short setae on all segments ending with 3 terminal
setae. The median flagellum 5-segmented, and end with 1 long
seta. Outer flagellum with 17 aesthetascs arranged in
3-3-3-3-3-2 on inner margin.
Antenna (Figure 4E). Antennal scale with 40 plumose setae.
Flagellum of antenna partially or completely divided into 14
segments.
Mandible (Figure 4F). Incisor process with 6 teeth; molar process finely serrated.
Maxillule (Figure 4G). Basal endite holding 2 sharp spines and
one seta. Coxal endite with 14 marginal spines and 4 mesial
spines. Apex with 2 setae.
Maxilla (Figure 4H). Partially or completely divided into 4
segments bearing 47 marginal setae and 7 mesial setae, 3-lobed
endite.
First maxilliped (Figure 5A). 5-segmented with dactylus bearing 6 plumose setae and 4–5 spines; propodus holding 24 hooked
setae arranged in 3 + 2 + 2 + 2 + 2 + 1 + 2 + 2 + 2 + 2 + 2 + 1 + 1, 2
mesial setae and 8 terminal setae; carpus with 21 marginal plumose setae; merus bearing 1 distal plumose seta.
Second maxilliped (Figure 5B). 5-segmented, with dactylus
bearing 4 teeth on occlusal margin; propodus with 48 denticles
and 3 proximal large spines on the inner margin.
Third maxilliped (Figure 4C). 5-segmented, with dactylus
bearing 3 short setae; propodus with 8–9 short setae and 5 spines;
carpus with 2 spines and 9 short setae.
Fourth maxilliped. 5-segmented, with dactylus bearing 2
short setae; propodus with 14 short setae and 5–6 spines; carpus
with 2 spines and 7 short setae.
Fifth maxilliped. 5-segmented, dactyl with 2 short setae; propodus with 2 spines and 7–9 short setae; carpus with 2 spines and
4 short setae.
Pereiopod I (Figure 5D). Pereopods 1–3, biramous unequally;
endopod unsegmented, shorter than exopod; exopod partially two
segmented.
Pleopod I (Figure 5E). Biramous; endopod with 31 plumose
setae, appendix interna with approximately 10 cincinnuli; exopod
with 30 plumose setae; 6 gill buds.
Pleopod II. Biramous; endopod with 39 plumose setae, appendix interna with ∼10 cincinnuli; exopod with 39 plumose setae; 7
gill buds.
Pleopod III. Biramous; endopod with 40 plumose setae,
appendix interna with ∼10 cincinnuli; exopod with 39 plumose
setae; 7 gill buds.
Pleopod IV. Biramous; endopod with 45 plumose setae,
appendix interna with ∼10 cincinnuli; exopod with 41 plumose
setae; 9 gill buds.
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Fig. 3. Neighbour-joining tree of 16S rRNA sequences of squilloid stomatopods. Branch length represents the Kimura 2-parameter distance. The terminal branches
of the same species are compressed from the original tree (see Supplementary Figure S1). Bootstrap values are shown on the nodes when >50. Arrow indicates the
position of the larvae examined.
Pleopod V. Biramous; endopod with 38 plumose setae, appendix interna with ∼14 cincinnuli; exopod with 32 plumose setae; 7
gill buds.
Uropod (Figure 5F). Protopodite terminating in 2 sharp
spines, inner longer; endopodite with 10 plumose setae on distal
margin; exopodite slightly longer than endopodite, basal segment
of exopodite with 5–6 marginal spines and apical segment with 20
plumose setae on distal margin. Distal margin of exopod reaches
over lateral tooth on telson.
Telson (Figure 4I). Well-developed with 1 submedian, 1 intermedian and 1 lateral tooth located on each side; 40 submedian
denticles, 9 intermedian denticles and 1 lateral denticles.
Colouration. The whole body, except for the retinal tissue, was
observed as transparent in life. Dark yellow to orange chromatophores were noticed on the mouthparts and a spot (each of which
has a combination of dark yellow to orange and dark red chromatophores) was observed on each side of the basal part of the fifth pleopods. The entire specimen turned white when preserved in ethanol.
Remarks. The propodus of the second maxilliped with three
basal spines; all five pleopods possessing an appendix interna
with cincinnuli; the exopod of uropod longer than endopod; the
telson with nine intermediate denticles.
Discussion
The K2P distance of the nucleotide sequences of 16S rRNA and/
or COI genes have been proposed as one of the indicators for species identification of stomatopods (Tang et al., 2010; Wong et al.,
2021). The distances to be found within the species are considered
below 2–2.4% for the COI gene and below 0.91–2.1% for the 16S
rRNA gene (Tang et al., 2010; Wong et al., 2021). The present
study also demonstrates that the K2P distance of 16S rRNA
gene can be considered 1% or lower within the species of
Squilloidea. Based on this indicator, our molecular analysis successfully assigned the two larval individuals to Levisquilla inermis
with <0.1% K2P distance. The closest relative of the L. inermis
clade was a congeneric species, L. jurichi, which was 3.4% K2P
distance from L. inermis. The K2P distance was sufficient to conclude that the two larval individuals are different species from L.
jurichi.
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https://doi.org/10.1017/S002531542100076X
Journal of the Marine Biological Association of the United Kingdom
Fig. 4. Levisquilla inermis (Manning, 1965), last-stage larva: (A) body (ventral); (B)
carapace (dorsal); (C) ventral view of carapace (left); (D) left antennule (dorsal); (E)
left antenna (dorsal); (F) left mandible (ventral); (G) left maxillule (ventral); (H) left
maxilla (ventral); (I) telson (dorsal). Scale bars: A, 5 mm; B, C, I, 1 mm; D–H, 200 μm.
Fig. 5. Levisquilla inermis (Manning, 1965), last-stage larva: (A) left first maxilliped
with enlarged portion of its distal end; (B) left second maxilliped; (C) left third maxilliped; (D) left first pereiopod; (E) left first pleopod with enlarged cincinnuli; (F) left
uropod (ventral). Scale bars: A, E, F, 1 mm; B, C, 0.5 mm; enlarged distal end, 300 μm;
enlarged cincinnuli, 40 μm.
There are three known species in the genus Levisquilla, namely
L. inermis, L. jurichi and Levisquilla minor (Jurich, 1904). Of
these, L. inermis is the only species reported to be from Japan,
including the Seto Inland Sea (Hamano, 1989, 2005; Ahyong,
2012). This species is also distributed in the other East Asian
countries, such as Korea and Taiwan (Ahyong et al., 2008;
Hwang, 2019; Hwang et al., 2019) while L. jurichi has also been
shown to occur in Korea (Hwang, 2019; Hwang et al., 2019),
and a L. jurichi post-larva was recently described as the first
record from Taiwan (Wong et al., 2021). These recent records
remind us of a possible appearance of L. jurichi larvae in
Japanese waters even though adults of the species are not yet
recorded there. However, sequences useful for DNA barcoding
were available in GenBank only for L. jurichi within the genus.
807
The addition of the sequence obtained from the adult specimen,
which morphologically strongly agreed with the previous studies
of L. inermis (Manning, 1965; Ahyong, 2001; Ahyong et al.,
2008; Ariyama et al., 2014) was the key factor to clearly solving
the assignment of the larvae into this species. At the same time,
our results support the assignment of the Taiwanese post-larva
to a group other than L. inermis even though L. inermis is the
only species from which the adult phase is known in Taiwan
(Ahyong et al., 2008; Wong et al., 2021). The K2P distance
between L. inermis and L. jurichi was confirmed as 3.4% in the
current study, which is much greater than the distance of 1.6%
(Wong et al., 2021) between their post-larva and the same
sequence of L. jurichi used for the analysis in this study.
Squilloid species have a propelagic stage with four pairs of
pleopods prior to entering the planktonic form of stomatopod
larva known as ‘alima’ with five pairs of pleopods (Manning,
1968; Ahyong et al., 2014). Some of the larvae pass through the
two propelagic stages before reaching the first pelagic stage
(Morgan & Provenzano, 1979). The alima is unique to
Squilloidea and is characterized by a telson with four or more
intermediate denticles, a propodus from the second maxilliped
with three basal spines, a long eyestalk, and the exopod of the uropod longer than the endopod (Gurney, 1942, 1946; Morgan &
Provenzano, 1979; Ahyong et al., 2014; Cházaro-Olvera et al.,
2018). Studies of pelagic larvae require not only the identification
of the species but also the identification of the developmental
stages, which makes the process so complicated that the progress
of larval biology is hampered. Indeed, the larval duration of stomatopods in the wild is not exactly known, and the number of
stages for wild-caught larvae of any provided species is approximate (Pyne, 1972). Our descriptions reveal that several diagnostic
features characterize the larvae: (1) well-developed pereiopod
characterized by the exopod partially or completely 2-segmented,
(2) maxilla partially or completely divided into 3 to 4 segments
with a 3-lobed endite, (3) apex of maxillule elongated and holding
two setae, and (4) well-developed uropod and distal margin of
exopod extend over lateral tooth on the telson. Those features
matched closely with the last larval stage of Oratosquilla oratoria
described by Hamano & Matsuura (1987). Thus, our larvae were
assigned to the last stage.
The Seto Inland Sea, which is a semi-enclosed coastal sea in
Japan, has various marine ecosystems that support a high level
of meroplankton diversity. The stomatopods, which constitute
one of the meroplankton communities in the Seto Inland Sea,
may play a role in maintaining the pelagic food chain. It is also
known that most stomatopod larvae inhabit coral reefs, and
they serve as predators of small reef fishes and invertebrates in
addition to serving as prey for predatory fishes, which reveal
the contribution of stomatopod larvae in maintaining coral reef
communities (Reaka et al., 2008; Abinawanto et al., 2019).
Besides that, larvae of the stomatopods provide an alternative
life stage to study biodiversity. Descriptions of 12 adult stomatopods from the Seto Inland Sea have been well documented by
numerous researchers (Ariyama, 1997, 2001, 2004; Hamano,
2005; Ariyama et al., 2014): (1) Lysiosquillina maculata
(Fabricius, 1793); (2) Cloridopsis scorpio (Latreille, 1828); (3)
Anchisquilla fasciata De Haan, (1833–1850); (4) Harpiosquilla
harpax (De Haan (1833–1850)); (5) Lophosquilla costata De
Haan, (1833–1850); (6) Oratosquilla oratoria De Haan, (1833–
1850); (7) Acanthosquilla multifasciata (Wood-Mason, 1895);
(8) Erugosquilla woodmasoni (Kemp, 1911); (9) Oratosquillina
perpensa (Kemp, 1911); (10) Levisquilla inermis (Manning,
1965); (11) Harpiosquilla melanoura Manning, 1968; and (12)
Clorida japonica (Manning, 1978). The study of stomatopod larvae from the Seto Inland Sea has been restricted due to the lack of
information for accurate taxonomic identification. The larvae of
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https://doi.org/10.1017/S002531542100076X
808
many species are yet to be identified, and the majority of work in
this area has been done on the commercial Japanese mantis
shrimp, Oratosquilla oratoria. Stomatopod larval life cycles usually involve several developmental stages, which are complicated
to identify without extensive morphological descriptions. This
study has demonstrated the capability of matching one developmental stage of our unknown larvae, obtained from the Seto
Inland Sea to species with a high degree of confidence by matching their DNA sequences with the DNA barcodes of the identified
adult. The results using this technique enable rapid species identification of stomatopod larvae and may encourage further studies
on stomatopod larval communities from the Seto Inland Sea for
which information is relatively inadequate. Furthermore, we provide some insights into the ecology of L. inermis since we found
both adult and larval specimens at the same location at the same
time, a finding that indicates that the Seto Inland Sea is one of the
main habitats of species settlement.
In conclusion, our data strongly link the larvae to their species
and confirm the occurrence of L. inermis in the Seto Inland Sea.
In addition, this study demonstrates the validity of the DNA barcoding method using the 16S rRNA gene for stomatopod larvae
identification from the Seto Inland Sea. Our study also reveals
that morphological identification should be supported with
molecular confirmation to accomplish a more accurate and legitimate result. Such a combination may encourage further taxonomic and ecological studies on stomatopod larvae.
Supplementary material. The supplementary material for this article can
be found at https://doi.org/10.1017/S002531542100076X
Acknowledgements. The authors express their gratitude to the captain and
crew of the ‘TOYOSHIO MARU’ (School of Applied Biological Science,
Hiroshima University) for specimen collection, to Mr Kenta Suzuki
(Graduate School of Integrated Sciences for Life, Hiroshima University) for
his courtesy of photographing the live materials during the cruise, and Ms
Chiho Hidaka (School of Applied Biological Science, Hiroshima University)
for her assistance in drawing and molecular work. Sequencing analysis was
performed at the Natural Science Center for Basic Research and
Development, Hiroshima University.
Author contributions. AEAF was responsible for the conceptualization of
the study, conceived and designed the experiments; performed the molecular
work and drawing; molecular and morphological analysis, interpreted the data,
and wrote the manuscript. SY and KW designed the collection of the specimens using the training and research vessel. SY made records of collection.
KW was responsible for the conceptualization of the study, molecular analysis,
supervision, wrote the manuscript, and research funding acquisition. All
authors reviewed the manuscript and approved the final version of it.
Financial support. This work was partly supported by the Promotion of
Joint International Research (Fostering Joint International Research)
(KAKENHI no. 17KK0157) awarded to KW.
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https://doi.org/10.1017/S002531542100076X