A new genus and species of Nannopodidae (Crustacea, Copepoda, Harpacticoida) from the Yellow Sea of South Korea
Author
Kim, Jong Guk
Marine Ecosystem Research Center, Korea Institute of Ocean Science & Technology, Busan 49111, South Korea
https://orcid.org/0000-0001-5299-9838
Author
Lee, Jimin
Marine Ecosystem Research Center, Korea Institute of Ocean Science & Technology, Busan 49111, South Korea
leejm@kiost.ac.kr
text
ZooKeys
2020
984
23
47
http://dx.doi.org/10.3897/zookeys.984.52252
journal article
http://dx.doi.org/10.3897/zookeys.984.52252
1313-2970-984-23
3BD22689146D4E3B9CFE6ACFB58F2778
AB8990636018519D824D455D3528A162
Concilicoxa hispida gen. et
sp. nov.
Figs 2
, 3
, 4
, 5
, 6
, 7
, 8
Type locality.
Off the Socheongcho Ocean Research Station (SORS) (
37°25'57.16"N
,
124°44'56.4"E
) in the Yellow Sea of South Korea, sandy sediments, 68 m depth.
Material examined.
Holotype
: SOUTH KOREA•♀ dissected and mounted on 11 slides; the Yellow Sea, off SORS;
37°25'57.16"N
,
124°44'56.4"E
; 68 m depth; 23 Mar 2018; Kim, J.G. leg.; sandy sediments; cat. MInRB-Hr59-S001.
Allotype
: SOUTH KOREA•♂ dissected and mounted on 11 slides; same data as for holotype; cat. MInRB-Hr59-S002.
Paratypes
: SOUTH KOREA•3♀♀2♂♂ dissected and mounted on 11 or 12 slides each; same data as for holotype; cat. MInRB-Hr59-S003-MInRB-Hr59-S007•3♀♀2♂♂ preserved together in 95% ethanol; same data as for holotype; cat. MInRB-Hr59-L001.
Other material for SEM.
SOUTH KOREA•2♀♀1♂ on a stub for SEM; same data as for holotype.
Description of holotype female
(MInRB-Hr59-S001). Total body length 617
μm
(measurement based on holotype and six paratypes: range = 530-626
μm
; mean = 588
μm
;
n
= 7); maximum width 86
μm
measured at the middle of cephalothorax. Body (Figs
2A, B
,
8A
) subcylindrical, slightly depressed, without distinct constriction between prosome and urosome; prosome slightly longer than urosome. Rostrum (Fig.
2C
) well-developed, triangular, reaching distal fourth of first antennular segment, defined from cephalothorax basally, with 1 pair of sensilla laterally and 1 median anterior pore ventrally; lateral margins convex proximally. Cephalothorax nearly square in dorsal aspect, slightly wider than long; integument covered with paired sensilla, several round depressions and irregular wrinkles (visible at high magnification, 1,000
x
; see insert in Fig.
2A
); posterior margin ornamented with short and fine setules; arthrodial membrane of first pedigerous somite visible dorsally and laterally. Tergites of somites with surface ornamentation composed of 1-3 transverse furrows, with 1 mid pore (absent in penultimate and anal somites) and 1 pair of lateral pores (absent in penultimate somite); posterior margins with several paired sensilla (absent in penultimate somite); hyaline frills weak, with 1 row of long setules posteriorly except for anal somite. Genital somite and first abdominal somite fused ventrally forming genital double-somite, but original segmentation indicated by internal chitinous rib dorsally and laterally; genital field (Fig.
3A, D
) with 1 large copulatory pore on midventral depression posterior to genital slit; genital slit reverse U-shaped, covered by 1 pair of large opercula derived from P6 on both sides; P6 represented by 1 long and 1 small seta, with 1 row of spinules subdistally; single midventral egg sac carrying 6 large eggs, as long as 1/4 of total body length. Anal somite (Figs
2A, B
,
3A, B
) with 1 pair of dorsal sensilla near base of operculum, 1 row of long setules on both ventrolateral margins; operculum semicircular, with smooth distal margin; anal opening with lateral row of small posterior spinules on each side; anal opening with 3 fringes of fine setules (Fig.
3B
).
Figure 2.
Concilicoxa hispida
gen. et sp. nov., female holotype (
A-C
)
A
habitus, dorsal
B
habitus, lateral
C
rostrum, dorsal. Male allotype (
D
)
D
habitus, dorsal.
Caudal rami (Figs
2A, B
,
3A-C
) elongate, oval, about 2.4 times as long as largest width, twice as long as anal somite; with a notch in mid-outer margin below caudal setae I and II; anterior half with a row of outer setules ventrolaterally; distal half with non-chitinous lateral margin; with 7 setae: seta I small naked, inserted in mid-length of outer margin ventrolaterally; seta II dorsal to and closely set to seta I, naked, longer than seta I; seta III naked, as long as seta II, arising from subdistal peduncle with 1 tube pore basally (Fig.
3C
); seta IV small, naked, slightly longer than setae II and III, fused to principal seta V basally; principal seta V well-developed, slightly longer than caudal ramus, ornamented with outer spinules distally; seta VI naked, as long as seta IV, inserted in outer distal corner; dorsal seta VII naked, tri-articulate at base, arising subdistally close to inner margin.
Figure 3.
Concilicoxa hispida
gen. et sp. nov., female holotype (
A-D
)
A
urosome, ventral
B
anal somite and caudal ramus, dorsal
C
caudal ramus, ventral
D
genital field, ventral. Male allotype (
E
)
E
urosome, ventral.
Antennule (Fig.
4A
) short, 4-segmented. First segment largest, elongate, as long as distal two segments combined, with 1 small naked seta subdistally; inner margin with short row of spinules subdistally; outer margin convex, with longitudinal row of minute spinules. Second segment smallest, with 3 bi-articulate and 5 naked setae; outer margin with 1 weak protuberance. Third segment about twice as long as second one, gradually widening distally; lateral margin with 3 bi-articulate and 3 naked setae; inner distal corner with 3 peduncles, of which two with 1 apical seta each, and one bearing 1 apical seta fused to basally to 1 ae. Distal segment as long as preceding one, tapering distally; lateral margins with 6 bi-articulate and 3 naked setae; distal margin with 1 naked seta and 1 acrothek composed of 1 ae and 2 bare setae. Setal armature as follows: 1-[1], 2-[8], 3-[8+ (1 + ae)], 4-[10 + acrothek].
Figure 4.
Concilicoxa hispida
gen. et sp. nov., female holotype (
A
)
A
antennule. Male allotype (
B
)
B
antennule.
Antenna (Fig.
5A
) with small, unornamented coxa (not shown). Allobasis elongate, 2.8 times as long as wide, exopod represented by 1 naked seta issuing at proximal third; abexopodal seta absent. Free endopodal segment with 1 short row of spinules subdistally and 1 surface frill distally; lateral armature composed of 2 weakly-serrate setae; distal armature comprising 1 small and 1 stout spine, 3 geniculate setae, innermost one of which fused basally to 1 small naked seta.
Figure 5.
Concilicoxa hispida
gen. et sp. nov., female holotype.
A
antenna (lacking coxa)
B
mandible
C
maxillule
D
maxilla
E
maxilliped.
Mandibular coxa (Fig.
5B
) slender, with 1 bulge and 1 row of spinules proximally; gnathobase well-developed, with 1 bicuspid and 3 unicuspid teeth, 1 small spinule and 1 unipinnate seta. Palp well-developed, uniramous; basis elongate, covered with rows of spinules, with 1 plumose seta distally; endopod 2-segmented, with 1 long plumose seta on proximal segment and 1 subapical and 2 apical setae on distal segment.
Maxillule (Fig.
5C
). Praecoxa with 1 row of outer spinules; arthrite with 1 naked seta on anterior surface and 7 spines on distal margin and ornamented with few long spinules on distal margin, 1 row of small spinules on dorsal margin and several spinules on posterior surface. Coxa armed with 1 row of outer spinules; endite elongate, with 2 elements distally and 1 row of small spinules laterally. Basis broad, with 2 endites: distal endite with 1 subapical and 3 apical setae; proximal endite incorporated into basis, represented by 2 long naked setae. Endopod incorporated into basis, represented by 3 long naked setae. Exopod 1-segmented, small, with 1 short and 1 long naked seta.
Maxilla (Fig.
5D
). Syncoxa armed with 1 row of stout spinules and 1 row of setules along outer margin, 1 row of minute spinules on surface and 1 patch of spinules near inner margin; with 2 coxal endites: proximal endite with 1 long naked seta and 1 short unipinnate seta (fused to endite basally); distal endite with 2 long naked setae and 1 unipinnate seta (fused to endite basally). Allobasis drawn out into strong claw with 2 accompanying naked setae and few spinules. Endopod incorporated into basis, represented by 2 long naked setae fused basally.
Maxilliped (Fig.
5E
) enlarged. Syncoxa elongate, ornamented with 1 group of spinules proximally. Basis elongate, about 3.4 times as long as maximum width, with 1 row of outer spinules proximally. Endopod drawn out into long and geniculate claw bearing 1 small accessory seta proximally.
P1 (Fig.
6A
). Praecoxa large, triangular, unornamented. Intercoxal sclerite broad, unornamented. Coxa wide, with outer margin forming 1 large and coarsely-serrated projection. Basis with 1 anterior pore and few spinules proximally; inner pedestal well-developed, with serrate distal margin; outer seta plumose, bi-articulated basally, arising from setophore ornamented with 1 row of small spinules at its base; inner seta naked, arising anteriorly, with 1 group of small spinules at its base. Exopod 2-segmented, short, about 0.3 times as long as enp-1; exp-1 with 1 naked outer seta and 1 row of stout outer spinules; exp-2 with 1 small naked seta and 1 stout unispinulose seta on outer margin and 1 short naked and 1 long geniculate seta on distal margin; anterior surface with 1 small pore. Endopod prehensile, 2-segmented; enp-1 elongate, 3.7 times as long as largest width, ornamented with 1 row of small spinules along outer margin and few long inner spinules; enp-2 short, slightly longer than wide, ornamented with few inner spinules and armed with 1 stout, recurved distal claw and 1 long flexible outer seta, of which distal half with very thin cuticular inner lines.
Figure 6.
Concilicoxa hispida
gen. et sp. nov., female holotype (
A-B
)
A
P1, anterior
B
P5, anterior. Female paratype (
C
)
C
abnormality of P2, anterior. Male allotype (
D-F
)
D
P3, anterior
E
P5, anterior
F
P6, anterior.
P2-P4 (Figs
7A-F
,
8B, C
). Protopods composed of praecoxa, coxa and basis. Praecoxae small, ornamented with 2 rows of spinules. Intercoxal sclerites large, broad, separate in P2, fused to coxae laterally in P3 and P4 (see arrowheads in Fig.
8B, C
). Coxae wide, with 1, 3 and 2 groups of spinules on anterior surface in P2-P4, respectively; outer margin drawn out into an elongate and coarsely-serrated projection. Bases wide, with 1 pore on anterior surface; outer setophore elongate, ornamented with 1 row of spinules basally, non-articulated in P2 with 1 plumose seta, bi-articulated in P3 and P4, with 1 naked seta; inner distal corner (near base of inner ramus) with 1 group of spinules. Exopod 1-segmented, ornamented with rows of spinules along outer and distal margins; with 4 stout outer spines, of which proximal one uniserrate and ornamented with 2 rows of setules, others pinnate; distal outer spines of P4 strongly pinnate. Endopod absent in P2, represented by 1 small unarmed protuberance in P3 and 1-segmented, ornamented with distal spinules and armed with 1 stout pinnate distal spine in P4.
Figure 7.
Concilicoxa hispida
gen. et sp. nov., female holotype
A
P2, anterior
B
protopod of P2, lateral
C
P3, anterior
D
protopod of P3, lateral
E
P4, anterior
F
protopod of P4, lateral.
P5 (Fig.
6B
). Baseoendopod broad, with 1 anterior pore, ornamented with rows of spinules along distal and inner margins; endopodal lobe weak, with 1 plumose distal seta; outer setophore articulate, with 1 long naked seta. Exopod small, with 3 pinnate setae and 1 naked seta.
Male
(allotype MInRB-Hr59-S002). Total body length slightly shorter than in female, 525
μm
(measurement based on allotype and 4 paratypes: range = 485-556
μm
; mean = 512
μm
, n = 5); body (Fig.
2D
) slightly more slender than in female, maximum width 74
μm
measured at the middle of cephalothorax; urosome 6-segmented, comprising P5-bearing somite, genital somite, 3 abdominal somites and anal somite; penultimate somite slightly shorter than its width, without lateral ornamentation. Caudal rami (Figs
2D
,
3E
) parallel, rectangular, more slender than in female; inner margin straight, outer margin slightly convex; outer margins unornamented, with clear cuticular inner line; additional large pore present on ventral surface; seta III issuing from subdistal lateral margin ventrally; set of setae I and II issuing from proximal third of outer margin; seta V slightly shorter than urosome (Fig.
2D
).
Antennule (Fig.
4B
) chirocerate, 5-segmented. First segment elongate, with 1 short naked seta subdistally; inner margin with few small spinules; outer margin convex, with 1 row of minute spinules. Second segment slightly longer than wide, with 2 bi-articulate and 7 naked setae and 1 minute protuberance. Third segment partially separated into two parts; proximal one with 2 bi-articulate and 6 naked setae; distal part with 2 setae. Fourth segment swollen, with 1 medial protuberance, 4 naked surface setae and 3 well-developed posterior penduncles: one proximal and one medial peduncle with 1 long naked apical seta each; subdistal peduncle with 1 long naked seta fused to 1 long ae basally. Distal segment elongate, slightly recurved distally, hook-shaped, with 2 naked and 6 bi-articulate setae laterally, 1 long naked seta distally and 1 acrothek composed of 1 ae and 2 naked setae fused basally. Setal armature as follows: 1-[1], 2-[9], 3-[10], 4-[6 + (1 + ae)], 5-[10 + acrothek].
P3 (Fig.
6D
) as in female, except for 1-segmented endopod with 1 stout distal spine bearing 2 pointed lateral processes.
P5 (Figs
3E
,
6E
) as in female except for anterior ornamentation with 2 rows of minute spinules.
P6 (Figs
3E
,
6F
) asymmetrical (one side completely fused to genital somite basally, other side articulated at base), each represented by a plate bearing 3 plumose setae and 1 row of minute spinules distally on inner extension.
Spermatophore as long as 4/5 length of P5-bearing and genital somites combined (Figs
2D
,
3E
).
Etymology.
The species epithet "
hispida
" is derived from the Latin adjective
hispĭdus
, which means
'hairy'
and refers to the setulose lateral ornamentation of the anal somite and caudal rami in the female. It is a noun in the feminine singular.
Variability and abnormality.
The investigated individuals of
Concilicoxa hispida
gen. et sp. nov. show intraspecific differences in appendage ornamentation. Dense spinular ornamentation was observed on the mandibular basis in one female paratype (MInRB-Hr-59-S003). This paratype also displays fusion of the coxa and basis of the P2 symmetrically (Fig.
6C
).
Remarks.
George (2002)
established the genus
Laophontisochra
to accommodate
L. maryamae
from the Patagonian continental slope (Chile) and
Laophontisochra
sp. from the Magellan Straits (Chile). He allocated this genus into the family
Cristacoxidae
Huys, 1990, based on the presence of an outward growth on the coxa of P1, an enlarged maxilliped and atrophy of the antennary exopod and abexopodal seta despite the discrepancies with the following characters of the family
Cristacoxidae
, which were defined by
Huys (1990)
: the first antennular segment with an outer spinous process, the absence of the exopod and an abexopodal seta in the antenna, the presence of modified seta on the middle endite of maxillary syncoxa and the single plate P5 with the same setae/spines in both sexes, which is considered as a neotenous origin.
George (2002)
suggested that the
Cristacoxidae
could be divided into two lineages: a plesiomorphic group comprising only
Laophontisochra
and a derived group composed of
Noodtorthopsyllus
Lang, 1965,
Cubanocleta
Petkovski, 1977 and
Cristacoxa
Huys, 1990 [the latter was considered as a junior synonym of
Noodtorthopsyllus
by
Huys and Kihara (2010)
]. However,
Huys and Kihara (2010)
transferred the genus
Laophontisochra
to the family
Nannopodidae
, based on a re-evaluation of the three fundamental morphological differences between the two groups suggested by George, with their newly-erected genus
Acuticoxa
within the family
Nannopodidae
for
Laophontisochra
sp. sensu George, 2002 (=
A. biarticulata
Huys & Kihara, 2010) and
A. ubatubaensis
Huys & Kihara, 2010 from the Brazilian coast. They assumed that both genera differ from the
Cristacoxidae
with the following evidence: (1) P1 coxa with a pair of serrated cristae (outer projections) in
Noodtorthopsyllus
and
Cubanocleta
vs. a single non-serrate, lobate or spinulose outgrowth in
Laophontisochra
and
Acuticoxa
; (2) maxillipedal endopod represented by a geniculated claw in
Laophontisochra
and
Acuticoxa
vs. non-geniculated in
Noodtorthopsyllus
and
Cubanocleta
; (3) antennary exopod consistently absent in
Noodtorthopsyllus
and
Cubanocleta
vs. atrophied in
Laophontisochra
and
Acuticoxa
(see
Huys and Kihara 2010
: 34). In addition,
Huys and Kihara (2010)
suggested that
Laophontisochra
and
Acuticoxa
are more closely related to both
Huntemannia
and
Rosacletodes
than to the cristacoxid genera, in that they share the presence of a coxal projection on the P1-P4 (vs. the plesiomorphic state of this character expressed in
Laophontisochra
, which lacks the coxal processes in the P2-P4).
Corgosinho (2012)
created the genus
Talpacoxa
, which was first mentioned as "Genus X" by
Huys and Kihara (2010)
and revealed close relationships amongst the genera of the nannopodid clade-
Huntemannia
,
Rosacletodes
,
Laophontisochra
,
Acuticoxa
and
Talpacoxa
-supported by three synapomorphies that are likely morphological adaptations to a burrowing lifestyle: (1) P1 coxa with an outer projection; (2) the P2-P4 exopods one- or two-segmented; and (3) the P2-P4 endopods one-segmented or vestigial.
The new genus
Concilicoxa
gen. nov. is assigned to the
Nannopodidae
because, as a member of the nannopodid clade, it exhibits the burrowing adaptation of the thoracopods.
Concilicoxa
gen. nov. appears to be closely related to both
Laophontisochra
and
Acuticoxa
in that they share four-segmented female antennules with elongate first segments, the prehensile P1 endopod, the presence of coxal outer projection on the P1, large and broad intercoxal sclerites on the P2-P4, the general shape of the female genital field (with a large copulatory pore and a well-developed operculum derived from P6) and elongate caudal rami. However, the novel genus is easily distinguishable from
Laophontisochra
by the distal armature of the antennary endopod with three geniculate and three non-geniculate elements (vs. four geniculate and two non-geniculate elements in
Laophontisochra
), the presence of coxal outer projections in the P2-P4 (vs. absent in
Laophontisochra
) and one-segmented exopods in the P2-P4 (vs. two-segmented in
Laophontisochra
). The new genus is also different from
Acuticoxa
in the absence of the P2 endopod (vs. one-segmented in
Acuticoxa
), a serrate coxal outer projection in the P1-P4 (vs. acute in
Acuticoxa
) and the female P5 exopod and baseoendopod separate (vs. fused into a single plate in
Acuticoxa
).
In contrast to a close resemblance with both genera in habitus and thoracopod morphology,
Concilicoxa
gen. nov. displays unambiguous autapomorphies that require the formation of a new genus: (1) the loss of the mandibular exopod, as observed in
Huntemannia
, is more derived than the exopod represented by a single seta; (2) the mandibular endopod is two-segmented, which seems to be secondarily divided, comparing to other related genera with only one-segmented endopod; (3) the P1exp-2 comprises a total of only four elements, but five or six setae in
Laophontisochra
and
Acuticoxa
, respectively (in the original description of
L. terueae
, this segment was described as having one lateral and three terminal setae, but was depicted as having three outer and three terminal elements; see
Bjoernberg
2014
: fig. 11A); and (4) the intercoxal sclerites of P3 and P4 are laterally fused with the coxae in
Concilicoxa
gen. nov. (Figs
6D
,
7C, E
,
8B-D
), but this fusion has rarely been reported in harpacticoid copepods (i.e.
Orthopsyllus
sp. of the family
Orthopsyllidae
Huys, 1990; cf.
Huys and Boxshall 1991
). By contrast, the presence of the maxillular exopod, as observed in
Talpacoxa
demonstrates a more plesiomorphic state than the lack of endopod.
Figure 8.
Concilicoxa hispida
gen. et sp. nov., scanning electron micrograph, female (
A-C
)
A
habitus, lateral
B
P3, anterior
C
P4, anterior. Male (
D
)
D
P3, anterior. Arrowheads indicate fusion of coxa and intercoxal sclerite.
The males of
Concilicoxa
gen. nov. exhibit distinctive potential autapomorphies for the genus as follows: (1) the P3 endopod has a sexual dimorphic distal element that is a robust spine; (2) the shape of P5 is nearly similar to that of the female; and (3) the caudal rami show sexual dimorphisms in the length of caudal seta V, the issuing position of setae I and II and the number of tube pores. However, we could not compare these characters with other related genera, because males of
L. maryamae
and
A. ubatubaensis
remain unknown. The sexual dimorphism of thoracopods is one of the most robust characters used to assess the phylogenic relationships between genera and between families because it facilitates comparison of the positions of homologue elements (such as setae or apophyses) of rami in females and males (
Huys 1990
;
Huys and Kihara 2010
). In this nannopodid clade, the known males tend to exhibit differences in morphology of the P3 endopod: (1) the male of
Rosacletodes
has a two-segmented P3 endopod with an elongate inner apophysis on enp-2, instead of a single seta as in the female (
Pallares 1982
); (2) all known males of the species of
Huntemannia
have an additional armature element on the P3 endopod, with no differences in segmentation as in
Nannopus
and
Pontopolites
(
Song et al. 2007
;
Karanovic and Cho 2018
); (3) the male of
T. brandini
exhibits a distal small apophysis on the one-segmented P3 endopod; and (4) although the male of
L. maryamae
has yet to be discovered, there is no sexual dimorphism on the P3 in
L. terueae
, whose taxonomic position seems to be problematic (see below). The male P3 endopod of the new genus presented herein is one-segmented with a stout spine (Figs
6D
,
8D
), whereas the female P3 endopod is represented by an unarmed protrusion. Such diverse sexual dimorphism of the P3 endopod prevents deeper insight into the systematic position of this clade within the
Nannopodidae
. We hypothesise that the lack of original outer element on the female P3 endopod in
L. maryamae
and
C. hispida
gen. et sp. nov. leads to the absence of the sexual dimorphic apophysis in the male. In contrast, the presence of a small apophysis on the corresponding ramus in
T. brandini
seems to be derived from a rudimental apical seta in the female.
Harpacticoids generally display sexual dimorphism in the size, shape and setae of the male P5. However, no sexual dimorphism has been observed in the male P5 of
Arenopontiidae
Martinez
Arbizu & Moura, 1994 (
Martinez
Arbizu and Moura 1994
). Additionally, both sexes bear the same number of setae/spines on the P5 of some taxa, such as
Metidae
Boeck, 1873,
Rotundiclipeidae
Huys, 1988,
Ectinosomatidae
Sars, 1903 and
Cristacoxidae
Huys, 1990 (
Huys 1988
;
Fiers 1992
;
Clement
and Moore 1995
;
Huys and Kihara 2010
). Except for
Ectinosomatidae
, the P5 of these families is remarkably reduced or represented by a single plate in both sexes. Although this sexual dimorphism is observed in other nannopodid genera, the structure of this leg in our new taxon is very similar in both sexes, except for micro-ornamentation, such as cuticular spinules and pores (Fig.
6B, E
). In addition, the male of
Concilicoxa
gen. nov. expresses rare sexual dimorphisms in the shape of the caudal rami (oval in the female, but rectangular in the male), the length of caudal seta V (slightly longer than the caudal ramus in the female, but slightly shorter than the urosome in the male), the number of pores on the surface (one pore in the female vs. two pores in the male) and the lateral ornamentation (the presence of a row of long setules proximally in the female vs. absent in the male). These sexual dimorphisms could support the erection of a new genus
Concilicoxa
gen. nov.