Crustaceana 88 (4) 449-465
A REVIEW OF NAUPLIAR DEVELOPMENT WITHIN THE
HARPACTICIDAE, WITH NAUPLIAR DESCRIPTION OF ZAUS
WONCHOELLEEI KANGTIA, DAHMS, SONG, MYOUNG, PARK & KHIM,
2014 (COPEPODA, HARPACTICOIDA)
BY
PAWANA KANGTIA1 ), HANS-UWE DAHMS2,3 ), SUNG JOON SONG4 ),
JUNG-GOO MYOUNG5 ) and JONG SEONG KHIM4,6 )
1 ) Faculty of Education, Bansomdejchaopraya Rajabhat University,
Bangkok 10600, Thailand
2 ) Department of Biomedical Science and Environmental Biology,
Kaohsiung Medical University, Kaohsiung 80708, Taiwan, R.O.C.
3 ) Department of Marine Biotechnology and Resources, National Sun Yat-sen University,
Kaohsiung 80424, Taiwan, R.O.C.
4 ) School of Earth and Environmental Sciences & Research Institute of Oceanography,
Seoul National University, Seoul 151-742, Republic of Korea
5 ) East Sea Research Institute, Korea Institute of Ocean Science and Technology,
Uljin 767-813, Republic of Korea
ABSTRACT
All six naupliar stages of the harpacticoid copepod Zaus wonchoelleei Kangtia, Dahms, Song,
Myoung, Park & Khim, 2014 are described. A key for the identification of the naupliar stages is
provided. Stages can be distinguished by number of segments of the exopod of antenna 2, setation of
the limbs including the bud of the caudal ramus, and presence and setation of the bud of maxilla 1.
In phylogenetic reconstructions there are several characters which link two taxa of different
harpacticoid groups, the Harpacticidae of Exanechentera and the Thalestridae of Podogennonta. The
Harpacticidae and the free-living genera of the Thalestridae develop from a 3-segmented naupliar
antennular precursor in Harpacticidae and a 1-segmented antennule in Thalestridae to a 6-segmented
antennule at copepodid I. Both families also share a single, stout spine terminally on the inner process
of the mandibular naupliar endopodite which is unique for harpacticoid nauplii. A peculiar medial
bifid seta on the antennal basis at nauplius I and II is also unique. This seta is replaced by a medial
seta of the coxa at nauplius III, which has the same structure as the aforementioned set which gets
reduced.
ZUSAMMENFASSUNG
Es werden alle sechs Naupliusstadien des harpacticoiden Copepoden Zaus wonchoelleei Kangtia,
Dahms, Song, Myoung, Park & Khim, 2014 beschrieben. Ein Schluessel zur Bestimmung der Naupliusstadien ist ebenfalls erarbeitet worden. Die Stadien koennen mit Hilfe der Aussenastsegmente
6 ) Corresponding author; e-mail: [email protected]
© Koninklijke Brill NV, Leiden, 2015
DOI 10.1163/15685403-00003423
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PAWANA KANGTIA ET AL.
von zweiter Antenne und Mandibel, der Beborstung aller Gliedmassen, sowie der Beborstung der
Maxilla und der urosomalen Anlage unterschieden werden. Phylogenetische Rekonstruktionen sind
dadurch kompliziert, dass es verschiedene Merkmale gibt, die 2 verschiedene Harpacticidengruppen
verbinden: die Harpacticidae der Exanechentera und die Thalestridae der Podogennonta. Alle Gattungen der Harpacticidae als auch die freilebenden Gattungen der Thalestridae entwickeln von einer
3-gliedrigen Naupliusantenne bei den Harpacticidae und einer 1-gliedrigen Naupliusantenne bei den
Thalestridae eine 6-gliedrige Antenne beim Copepoditen I. Beide Familien haben darueber hinaus
einen separaten, kurzen Dorn terminal am inneren Anhang des mandibularen Endopoditen. Eine mediale gegabelte Borste an der Basis der zweiten Antenne nur beim Nauplius I und II ist ebenfalls
einzigartig fuer die Harpactioida. Diese Borste an der Basis wird ersetzt durch eine aehnliche Borste
an der Coxa beim Nauplius III in beiden Familien.
INTRODUCTION
Detailed and exact descriptions of postembryonic instars are especially needed
for the elucidation of phylogenetic relationships within the Copepoda (Dahms,
1990a, b). High resolution is a prerequisite for meaningful comparison, since
phylogenetically valuable apomorphies may be cryptic characters which are often camouflaged by superficial resemblances (Dahms, 1992, 1994; Dahms & Fernando, 1992, 1993a, b, 1995a). But detailed studies are the more difficult the more
complicated or smaller a structure is. This is especially true for minute nauplii,
many of which do not exceed 50 μm in diameter at hatching. Current knowledge
of phylogenetic relationships is mainly based on what can be deduced from adult
morphology (Dahms, 1992). However, evidence from postembryonic stages should
complement that gained from adult characters for a species exhibits different and
significant characters at all phases of its ontogeny and these can be used as speciesspecific character patterns of evolutionary species (Dahms, 2000, 2004).
MATERIAL AND METHODS
Collection data.— Ovigerous females of Zaus wonchoelleei Kangtia, Dahms,
Song, Myoung, Park & Khim, 2014 which provided the developmental stages were
collected from a seaweed Padina sp. at Tongyeong Sea Cage Area (34°47.47 N
128°21.49 E). They were placed in a beaker in which substratum from the field
was stirred up, and subsequently decanted over a screen (mesh size 100 μm).
The residue containing, e.g., harpacticoids was rinsed into smaller bowls for
transport to the laboratory. The developmental stages used in this study exclusively
represent the offspring of single-female cultures, unless indicated otherwise. The
classification used is that of Lang (1948, 1965).
Cultivation.— Ovigerous females of Zaus wonchoelleei were transferred to
individual Petri dishes containing filtered sea water. These were kept at 2024°C with a light-dark cycle of 12/12 h. Water renewal was about 50% per
NAUPLII OF ZAUS WONCHOELLEEI (COPEPODA, HARPACTICIDAE)
451
week. Seawater was obtained and prepared as described by Dahms (2000). When
nauplii emerged, some of them were isolated in watch glasses and the exuviae
of subsequent moults were collected. Dunaliella salina (Dunal) Teodoresco, 1905
was used as algal food. A few drops of food-suspension were added every few
days.
Preparation.— Stages were fixed in 5% buffered formaldehyde and embedded
in glycerine which clears the natural colour of nauplii, and colour and shape of
the red nauplius eye is lost quite soon and the eye is, thus, not figured. Nauplii
were mounted whole, broken cover-glass pieces being added to prevent them from
being compressed and to facilitate rolling to allow inspection from all sides. Body
lengths were measured from the anterior to the posterior end of the naupliar body:
body width is given as the widest part of the nauplius. Drawings were made from
single specimens; others (2-5) were checked for variability. The specimens have
not been stained and that the naupliar appendages have not been dissected due to
the small size of the nauplii.
Descriptive terminology.— The following terms are defined according to their
usage in the following sections of this paper: The harpacticoid nauplius has at
least three pairs of appendages: the antennules, antennae and mandibles. The body
is completely covered by a usually smooth nauplius shield in the earlier stages,
whereas the hind-body protrudes from it in later stages. At the posterior end of the
body there is at least one caudal seta on both sides of the anal area. The labrum
originates as a lobular flap near the frontal margin of the body, between the bases
of the antennules, and extends posteriorly across the ventral surface of the body.
The ventral body wall is a tongue-like structure arising at the base of the antennal
protopodite. The antennule is uniramous. The antenna is noticeably different from
that of the adult (and copepodids) in having a precoxa in some cases and a naupliar
arthrite. The antenna further consists of a coxa, basis, endopodite and exopodite.
The mandible is composed of the same elements. The endopodite consists of an
inner process and usually an outer lateral field of setae arising on the outer lateral
margin (except in Polyarthra where it is homologous to the 2nd segment and in
Ectinosomatidae where it is vestigial). The postmandibular appendages (maxillule,
maxilla, maxilliped, leg 1 and leg 2) may develop successively from nauplius II
onwards. For all appendages the singular form is used. Large outgrowths are called
setae or spines. A typical seta is generally a flexible, finely attenuate element which
is bare or has a double row of fine hair-like outgrowths. In the latter case it is called
pinnate, or, if the fine spinules are more irregular, it is called spinulose. The typical
spine is generally short, relatively inflexible, and usually bears a double row of tiny
spinules. Very small elements usually originating as extensions of the epicuticle are
referred to as “setules” but only if they originate from the epicuticle of a seta.
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PAWANA KANGTIA ET AL.
Aesthetascs (aesthetes sensu Nishida & Ohtsuka, 1997) are presumed sensory
elements of the antennule with sclerotized bases and are more transparent than
normal setae with blunt or rounded ends. The complement of setae, setules, spines
and aesthetascs is called element of a particular structure and is referred to as the
armature. In addition to setae, setules and spines, the body segments or appendages
present a variety of ornamenting cuticular projections. Spinules could be very fine
hair-like cuticular extensions of setae and spines, labrum and ventral body wall, or,
small, pointed, conical processes. Denticles are minute triangular outgrowths. The
spinules and denticles are considered as the ornamentation.
RESULTS
Description of naupliar stages of Zaus wonchoelleei
The nauplii of Zaus wonchoelleei (figs. 1-7) have naupliar shields which are
bare. Hind-body bears 1 seta on either side at nauplius I and nauplius II, 3 at
nauplius III, 4 at nauplius IV and nauplius V, and 5 setae at nauplius VI. At
nauplius V a protuberance with a pore at tip arises between uttermost seta and
biarticulated dorsal one. A row of long subterminal spinules is present at caudal
edge at nauplius I and nauplius II. Spinules are reduced in size but increase in
number at nauplius II when anal area becomes indented. Spinules are scattered
around the proximal part and subterminal part on caudal area. Anal-operculum
is rounded and bare. Labrum is oval-shaped with spinule-row around lateral and
caudal edge.
Nauplius I
Body slightly longer than wide with cephalic shield. Body length 112 μm, body
width 100 μm. Antennule (fig. 4A) 3-segmented. Segment 1 unarmed, segment 2
with 2 small and 1 long medial seta distally with longer spinules distally which
are extended caudally. Segment 3 with 1 subterminal seta and 2 long setae and an
aesthetasc distally.
Antenna (fig. 5A) with coxa and basis, 4-segmented exopod and 1-segmented
endopod. Coxa with row of denticles dorsally and 1 small seta and naupliar arthrite
with 4 setae distally. Basis with setule row dorsally, with 1 thick seta bearing bifid
tip and tiny setules on it, and with 2 bare setae. Exopod is shorther than endopod;
segment 1 without ornamentation, segment 2 longest with 2 setae, and segments 34 with 1 and 2 setae, respectively. Endopod robust with 1 inner bare seta on middle,
and with 1 stout claw bearing setule row on inner margin.
Mandible (fig. 7A) with coxa and basis. Coxa with 1 inner seta. Basis with
1 inner seta bearing setule row on inner margin, and 2 setule rows dorsally.
Exopod 1-segmented, with 1 lateral seta proximally and 2 setae distally. Endopod
NAUPLII OF ZAUS WONCHOELLEEI (COPEPODA, HARPACTICIDAE)
453
Fig. 1. Zaus wonchoelleei Kangtia, Dahms, Song, Myoung, Park & Khim, 2014, habitus. A,
Nauplius I, ventral view; B-D, nauplius II, ventral, lateral and dorsal view, respectively.
1-segmented, with 3 outer setae and 1 stout spine bearing a setule row along inner
margin.
Nauplius II
Differing from nauplius I in size and as follows: Body (fig. 1B-D) as long as
wide and of circular form.
Antennule (fig. 4B), segment 2 with 1 long medial seta between 2 bare setae.
Antenna (fig. 5B), coxal naupliar arthrite well developed with denticles distally
but without dorsal spinules. Basis with more setules dorsally, 1 thick seta modified
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PAWANA KANGTIA ET AL.
Fig. 2. Zaus wonchoelleei Kangtia, Dahms, Song, Myoung, Park & Khim, 2014, habitus. A,
Nauplius III, ventral view; B, nauplius IV, ventral view.
bearing sharp tip. Exopod with 1 lateral seta added to segment 2. Endopod with 2
tiny setae added to inner margin and outer distal corner.
Mandible (fig. 7B). Basis with reduced dorsal setules. Exopod-2segmented,
segment 1 unarmed, segment 2 with 1 bare seta proximally and 2 distal setae added.
Endopod with 1 outer seta added.
Maxillule (fig. 1B, D) reprensented by 1 seta.
Nauplius III
Differing from nauplius II in size and as follows: Body (fig. 2A) length 120 μm,
body width 112 μm.
NAUPLII OF ZAUS WONCHOELLEEI (COPEPODA, HARPACTICIDAE)
455
Fig. 3. Zaus wonchoelleei Kangtia, Dahms, Song, Myoung, Park & Khim, 2014, habitus. A,
Nauplius V, ventral view; B, nauplius VI, ventral view.
Antennule (fig. 4C), segment 2 with setule row outerodistally, segment 3 with 8
setae added (now 11 + ae).
Antenna (fig. 5C), coxal naupliar arthrite well developed, and coxa with 1 seta
bearing bifid tip (now 2 setae). Basis with 4 bare setae in total. Exopod segments 2
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PAWANA KANGTIA ET AL.
Fig. 4. Zaus wonchoelleei Kangtia, Dahms, Song, Myoung, Park & Khim, 2014. Antennule of
nauplius I-VI.
NAUPLII OF ZAUS WONCHOELLEEI (COPEPODA, HARPACTICIDAE)
457
Fig. 5. Zaus wonchoelleei Kangtia, Dahms, Song, Myoung, Park & Khim, 2014. Antenna of
nauplius I-IV.
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PAWANA KANGTIA ET AL.
Fig. 6. Zaus wonchoelleei Kangtia, Dahms, Song, Myoung, Park & Khim, 2014. Antenna of
nauplius V-VI.
and 4 with 1 more bare seta, respectively (now 4 and 3). Endopod with 1 small seta
added to inner margin.
Mandible (fig. 7C), endopod with setule row subdistally and 1 outer seta added
(now 5).
Maxillule (fig. 2A) with 2 setae on small protuberance in total.
NAUPLII OF ZAUS WONCHOELLEEI (COPEPODA, HARPACTICIDAE)
459
Fig. 7. Zaus wonchoelleei Kangtia, Dahms, Song, Myoung, Park & Khim, 2014. Mandible of
nauplius I-VI.
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PAWANA KANGTIA ET AL.
Nauplius IV
Differing from nauplius III in size and as follows: Body (fig. 2B) length 136 μm,
body width 129 μm.
Antennule (fig. 4D), segment 3 with 1 more seta (now 12 + ae).
Antenna (fig. 5D), exopod segment 1 with setules on surface, segment 2 with
setules on surface. Endopod with 1 tiny seta added on inner margin.
Mandible (fig. 7D) remains unchanged.
Maxillule (fig. 2B) with 3 setae on small protuberance in total.
Nauplius V
Differing from nauplius IV in size and as follows: Body (fig. 3A) length 164 μm,
body width 153 μm.
Antennule (fig. 4E) and antenna (fig. 6A) same as at nauplius IV.
Mandible (fig. 7E), with setule row dorsally on basis.
Maxillule remains unchanged and is not figured.
Nauplius VI
Differing from nauplius V in size and as follows: Body (fig. 3B) length 194 μm,
body width 177 μm.
Antennule (fig. 4F) and mandible (fig. 7F) same as nauplius V.
Antenna (fig. 6B), coxal naupliar arthrite absent and with only 1 inner seta
proximally. Basis with 3 inner setae totally. Endopod with setule row added on
dorsal surface and 1 inner proximal seta absent (now 2 on inner margin).
Intraspecific variability
Variability was observed in the number of spinules, the length of setae and
body size in general. Variability of ornamentation is not only restricted to different
individuals but was also different for the two sides of the body.
K EY
TO
NAUPLIAR S TAGES
OF
Zaus wonchoelleei
1. Almost circular in shape; 1st maxilla not indicated . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nauplius I
– 1st maxilla appears as 1 seta or a setose bud . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. 1st maxilla appears as 1 seta; not more than 2 caudal setae on each side . . . . . . . . . . Nauplius II
– More than 2 caudal setae on each side . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Four (4) caudal setae on each side . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nauplius III
– More than 4 caudal setae on each side . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
4. 1st maxilla present as lobe with 3 setae; no indication of leg 1 . . . . . . . . . . . . . . . . . . Nauplius IV
– Indication of leg 1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5. Leg 1 indicated as an abdominal fold without setal armature . . . . . . . . . . . . . . . . . . . . Nauplius V
– Legs 1 and 2 indicated as abdominal lobes, each bearing setal armature . . . . . . . . . Nauplius VI
NAUPLII OF ZAUS WONCHOELLEEI (COPEPODA, HARPACTICIDAE)
461
DISCUSSION
As far as naupliar development is concerned in the Harpacticidae, Tigriopus
is studied best by workers like Guiglia (1926), Fraser (1936) and Shaw (1938),
studying T. fulvus (Fischer, 1860). Igarashi (1963), Ito (1970) and Koga (1970)
studied the nauplii of T. japonicus Mori, 1938. Nauplii of the genus Harpacticus
are known from a rough drawing of an early nauplius of H. uniremis Krøyer, 1842
by Brian (1919), from a single nauplius of H. littoralis Sars G. O., 1910 by Griga
(1960), from the first 5 nauplii of the same species by Castel (1976) and from
the detailed study by Walker (1981) on Harpacticus sp. The nauplius I of Zaus
spinatus Goodsir, 1845 is shown by Lang (1948) and the first 5 nauplii of the same
species are described by Clogston (1965).
The main characteristics of Zaus wonchoelleei, Zaus and the Harpacticidae are
discussed below.
Reduction of feeding parts.— The reductions at nauplius VI in all the parts of
the body being involved in feeding which are characteristic for the family are only
reported by Itô (1970) for T. japonicus and by Walker (1981) on Harpacticus sp.
All other authors do not mention any reductions in the text and figure and the
nauplius VI is unchanged showing an unchanged masticatory apparatus.
Mandibular endopodite.— The mandible endopodite is elongate and bears an inner process armed with 1-2 terminal curved setae and usually an outer lateral bulge
bearing 3-4 setae at nauplius I in Exanechentera and Podogennonta augmented to
5 or 6 in later stages. In Ectinosomatidae (as in Miracidae and Metidae) this bulge
is represented by a small protuberance at nauplius I which is completely reduced
in later stages. Phyllognathopus viguieri (Maupas, 1892) has an endopodite similar to that of the more advanced sections of Oligoarthra. Development of only 1
spiniform seta terminally on the inner process of endopodite is restricted to the following families: Harpacticidae, Thalestridae, Miracidae and Metidae. They belong
to the thalestridimorph and metidimorph taxa of Podogennonta except Harpacticidae which belong to the Exanechentera.
Segmentation of antennal and mandibular exopodite.— According to Walker
(1981) in Harpacticus sp. is any segmentation lacking on both, the antennal and
mandibular exopodite throughout the phase. This is in contrast to the present
observation of a 3-segmented antennal and a 1-segmented mandibular exopodite
in H. uniremis which is confirmed by Castel (1976) on H. littoralis. Clogston
(1965) described the antennal exopodite of Zaus spinatus as being 2-segmented
throughout the phase whereas it is 4-segmented in the present study. Clogston has
missed nauplius II and describes the nauplius III as the nauplius II, nauplius IV
as nauplius III and so forth until he misinterpreted the nauplius VI stage as
nauplius V. Clogston (1965) shows an indication of the reduction process of the
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PAWANA KANGTIA ET AL.
oral appendages but in contrast to the present report it is said that there is no
indication of the maxilla. The interpretation of 2 spinule rows on either side of the
ventral hind-body of nauplius III of Harpacticus sp. (Walker, 1981) as rudiments
of legs 1 and 2 is doubted here.
Appearance of postmandibular appendages.— As for the postmandibular appendages labeling the exuvial rudiments as they appear in the developmental sequence as maxillulae, maxillae etc. should not be considered a reliable method
because a suppression of Anlagen can occur within this series (as the maxilla in
Polyarthra and Zaus spinatus). It has to be born in mind that chitinous structures
at least within the Harpacticoida are observed to be modified only through moults.
Before each moult the underlying tissue forms the Anlagen of both modified and
unmodified structures. It is not always easy to identify outer chitinous structures
with their potential precursors formed under the cuticle because the same tissue
may form different chitinous structures. Sometimes anatomical changes under the
cuticle (formation of segments, buds of appendages) remain hidden there, not being expressed on the outside should be correlated with the exuvial Anlagen — if
they are present-to verify their identity. This, however, may require histological
studies in most of the cases.
Similarity between nauplii and copepodids.— As for the similarity between
nauplii and copepodids, nauplii of Zaus spinatus bear a spinule fan on the antennal
endopodite claw and on the seta of the mandibular endopodite process. Such a fan
also exists on the copepodid endopodite leg 1 of this species.
Phylogenetic relationship between Harpacticidae and Thalestridae.— Phylogenetic reconstructions need to consider that there are several characters which link
two taxa of different “subsections” (according to Lang, 1948): the Harpacticidae
of Exanechentera with the Thalestridae of Podogennonta. To our knowledge this
situation has so far passed unnoticed. However, this case is of conflicting evidence. All known genera of the Harpacticidae and the free-living (1) genera of
the Thalestridae have a 6-segmented antennule at C I. This is a very peculiar character not known from any other harpacticoid species (Dahms, 1989). At C II, a
7-segmented antennule is acquired bearing the aesthetasc on segment 2 in both
families Harpacticidae and Thalestridae. The 6-segmented antennule of C I develops from a 3-segmented naupliar precursor in the Harpacticidae but from a 1segmented naupliar antennule in the Thalestridae. But, as shown by Pseudotachidius sp. and Xouthous (= Idomene) sp., a 3-segmented naupliar antennule is present
in the Thalestridae as well (in case both these taxa are not to be removed from the
Thalestridae for their otherwise derived characters).
The most specific naupliar character is the single, stout spine terminally on the
inner process of the mandibular endopodite. This character is common to both,
NAUPLII OF ZAUS WONCHOELLEEI (COPEPODA, HARPACTICIDAE)
463
Harpacticidae and Thalestridae (and for the Miracidae and Metidae belonging to
the Thalestridimorpha) whereas it is not present in any other harpacticoid.
Furthermore, in both taxa (and in the Miracidae) a bifid seta is found medially
on the coxa of nauplius III and later stages. The bifid seta on the basis of nauplius I
and II is replaced by a simple seta of reduced length in nauplius III-VI. This
then has the same structure as the aforementioned seta which itself is reduced
in size and shape. Other common characters in species of the Harpacticidae and
Thalestridae are as follows: the distal seta of the second antennular segment is
long and bears long spinules distally (however, this is also indicated in the tisbids
Scutellidium hippolytes (Krøyer, 1863) and in Tisbe bulbisetosa Volkmann-Rocco,
1972) and the antennal masticatory process is heavily toothed. Another similarity
is the presence of 2 setae with common base on the mandibular exopodite in
some representatives at least (so in Harpacticus uniremis and Zaus spinatus for
Harpacticidae and Parathalestris harpactoides (Claus, 1863) for Thalestridae).
However, this character is also found in Tisbidae (see below).
As many of their representatives are phytal living forms, one could argue that
both, Harpacticidae and Thalestridae have evolved these characters independently.
However, as will be shown later, judged from larval evidence the Thalestridae
are in good agreement with the taxa placed on the “thalestridimorph branch” by
Lang (1948). Therefore, the Thalestridae should not be reallocated. A removal of
the Harpacticidae from the “Tachidiidimorpha” would be more easily justified.
The main argument against this is the peculiar reduction of the oral parts at
nauplius VI uniting the Harpacticidae with the Tachidiidae. All that can be done
for the moment is to emphasize the similarity of characters of both taxa demanding
further investigation to clarify the relationships of Harpacticidae and Thalestridae.
ACKNOWLEDGEMENTS
The first three authors, Pawana Kangtia, Hans-Uwe Dahms, and Sung Joon
Song, contributed equally to the manuscript. This research was supported from the
project titled ‘Development of integrated estuarine management system’, funded
by the Ministry of Oceans and Fisheries, South Korea. This research was a part of
the project titled “Integrated management of marine environment and ecosystems
around Saemangeum” funded by the Ministry of Oceans and Fisheries, South
Korea.
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First received 23 May 2014.
Final version accepted 3 March 2015.