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Zelinkaderes yong sp. nov. from Korea - the first recording of Zelinkaderes (Kinorhyncha: Cyclorhagida) in Asia
Zoological Studies volume 54, Article number: 25 (2015)
A new kinorhynch species, Zelinkaderes yong sp. nov., is described from Korea.
Zelinkaderes yong sp. nov. is described from coastal, sandy habitats in Korea by means of light and scanning electron microscopic techniques. The new species is characterized by the presence of cuspidate spines in lateroventral positions on segments 2 and 9, ventrolateral positions on segment 5, and lateral accessory positions on segment 8; flexible tiny acicular spines in lateroventral positions on segment 2, more regular-sized lateroventral acicular spines on segment 8, and middorsal spines on segments 4, 6, 8, 9, and 11. Females furthermore have acicular spines in middorsal and midlateral positions on segment 10, whereas males have crenulated spines on this segment. The absence of acicular spines in the lateral series of segment 9 makes it easy to distinguish the new species from all previously described congeners. The new species differs most from Zelinkaderes submersus, whereas it is morphologically closest to Zelinkaderes klepali. In regard to the spine patterns, the new species only differs from Z. klepali by its lack of lateroventral acicular spines on segment 9.
The finding of a new species of Zelinkaderes in East Asia extends the distributional range of the genus, which suggests that the genus basically could be present anywhere in the world and could be considered as cosmopolitan.
Kinorhynchs are small, worm-like, invertebrate animals that live among the marine meiobenthos. They have been known since 1851, but knowledge about their diversity is still incomplete (Dujardin 1851; Neuhaus 2013). The current number of 217 valid described species (based on description of adult specimens) is expected to increase substantially by intensified research efforts (Sørensen 2013). South Korea is one of the countries where kinorhynch diversity is relatively well known with more than ten new species discovered within the last 4 years (Sørensen et al. 2010a; Sørensen et al. 2010b, c; Lundbye et al. 2011; Sørensen et al. 2012; Sørensen et al. 2013).
The family Zelinkaderidae and genus Zelinkaderes were described in 1990 by R. P. Higgins (1990). Members of the genus are characterized by the presence of 16 indistinct placids on the neck that are basally fused with the first trunk segment. The first and second trunk segments consist of complete cuticular rings, whereas the third to tenth segments are composed of single plates with midventral articulations. Oral styles are bipartite; middorsal spines are present on segments 4, 6, and 8 to 11; cuspidate spines are found on several segments; and a midterminal spine is present. Currently, Zelinkaderidae accommodates two genera: Triodontoderes (see Sørensen and Rho 2009) with one species and Zelinkaderes (see Higgins 1990) with four previously described species. The first Zelinkaderes species to be discovered was actually described as Cateria submersa Gerlach 1969. This species was found in medium coarse sand near Helgoland in Northwest Germany (Gerlach 1969). However, this species was later redescribed by Higgins (1990) and assigned to the new genus, Zelinkaderes, under the name Zelinkaderes submersus (Gerlach 1969). In the same contribution, Higgins (1990) reported a second species of the genus, Zelinkaderes floridensis Higgins 1990, that was collected from localities with muddy sand, around 20 miles off Fort Pierce at the Atlantic Coast of Florida. Only 6 years later, Bauer-Nebelsick (1995) described a third species, Zelinkaderes klepali Bauer-Nebelsick, 1995, from coral sand at the Egyptian Red Sea coast. The fourth, and until now most recently discovered species, Zelinkaderes brightae Sørensen et al., 2007, was also described from Fort Pierce, Florida but from much cleaner calcareous sand than Z. floridensis and also closer to the coast. The type locality of Z. brightae is situated 6 miles off Fort Pierce (Sørensen et al. 2007), but subsequently, Herranz et al. (2013) have recorded the species at localities only 3 and 4 miles from the coast. Generally, the taxonomy of Zelinkaderes appears to be relatively uncomplicated, and the four known species can be distinguished by their lateral spine patterns and in particular by the position of their cuspidate spines.
In the present contribution, we describe the fifth species of Zelinkaderes. This species is the first intertidal species known from the genus, and it also represents the first Asian recording of the genus.
Specimens of Zelinkaderes yong sp. nov. were collected at two localities. The holotype and some paratypes were collected by scuba diving on 7 September 2001 from subtidal sand on 3- to 6-m depth at Guryongpo, near Pohang (Figure 1A) on the east coast of the Korean Peninsula (position: 36° 00′ 06″N, 129° 34′ 17″E). Additional paratypes were collected on 15 May 2010 from intertidal sand around Shinchang (Figure 1B) on the west coast of Jeju Island in South Korea (33° 20′ 42″N, 126° 10′ 12″E). At this second locality, the water retracts completely from the area at low tide. The substrate was fine sand with lots of crustacean tubes (Callianassa japonica (Ortmann 1891)). Specimens at this locality were collected by digging a small pit into the sand and sieving the accumulating water with a net of 100-μm mesh size. The specimens occurred in so high numbers that no further extraction was required.
All collected specimens were fixed in 4% formalin buffered with sea water. For light microscopy, fixed specimens were transferred to distilled water, dehydrated through a graded series of glycerin, and mounted in Fluoromount G® on glass slides. They were examined using an Olympus BX51 microscope equipped with an Olympus DP20 camera and Normarski differential interference contrast optics. Measurements were made with Cell^D software version 2.7. (Olympus A/S, Ballerup, Denmark).
For scanning electron microscopy (SEM), specimens were dehydrated using a graded series of ethanol, transferred to acetone, and finally critical point dried. Dried specimens were mounted on aluminum stubs, sputter coated with a platinum/palladium mix, and examined with a JEOL JSM-6335 F field emission SEM (JEOL GmbH, Eching, Germany).
Type material is stored at the Natural History Museum of Denmark.
Family ZELINKADERIDAE Higgins 1990
Genus ZELINKADERES Higgins 1990
Type species Zelinkaderes yong sp. nov.
Etymology: Like several other mud dragon species, this one is named after a dragon. The species name ‘yong’ refers to a dragon in Korean mythology.
Holotype: Adult male from Guryongpo, near Pohang on the East coast of the Korean Peninsula; 7th September 2001: 36° 00′ 06″N, 129° 34′ 17″E, in subtidal sand from 3- to 6-m depth, mounted in Fluoromount G®, deposited at the Natural History Museum of Denmark (NHMD) under accession number: ZMUC KIN-000818.
Paratypes: two adult females, three adult males, and one juvenile, collected at same time and locality as the holotype, mounted in Fluoromount G®, and deposited at the NHMD under accession numbers: ZMUC KIN-000819 to KIN-000824. Additional paratypes include seven adult females and two adult males, collected from an intertidal sand flat at Shinchang, Jeju Island, South Korea; 15th May 2010: 33° 20′ 42″N, 126° 10′ 12″E, mounted on an SEM stub and deposited at the NHMD under accession number: ZMUC KIN-000825.
Zelinkaderes sp. in Park et al. 2006; Zelinkaderes sp. JKP-2005: 18S rRNA sequence (accession number AY746985) in GenBank (NCBI).
Zelinkaderes yong sp. nov. has middorsal spines on segments 4, 6, and 8 to 11 (middorsal spine on segment 10 crenulated in males), lateroventral cuspidate spines on segments 2 and 9, lateral accessory cuspidate spines on segment 7, ventrolateral cuspidate spines on segment 5, lateroventral acicular spines on segment 8, and midlateral spines on segment 10, as regular acicular spines in females and crenulated spines in males. Lateral terminal spines, lateral terminal accessory spines, and midterminal spine are present on segment 11. Large sensory spots are present middorsally on segment 2, midlaterally on segments 2, 6, and 7, sublaterally on segments 4 and 9, subdorsally and lateroventrally on segment 10; smaller sensory spots are present in paradorsal positions around dorsal spines and in ventrolateral positions on segment 11. Trunk segments 1 to 10 have cuticular hairs arranged in a longitudinally striated pattern with distinct hairless patches midlaterally on segments 3 to 7 and 9. Segment 11 has cuticular hairs not arranged in any particular pattern.
Adult specimens possess a head, neck, and 11 trunk segments (Figures 2A,B and 3). The trunk appears long, thin, and vermiform with a semicircular cross section and a slight thickening of the trunk in the middle (Figure 4A). Trunk segments 1 and 2 are composed of closed cuticular rings and segments 3 to 11 of a single plate with a midventral joint (Figure 2B). The midventral joint appears as a distinct cuticular surface marking on segments 3 to 10, whereas it is only an intracuticular line on segment 11. The anterior border of all segments is straight. An extremely weak pectinate fringe is present on the posterior edges of segments 1 to 10. The cuticle is patterned by longitudinal furrows populated with cuticular hairs (Figure 4B). The midterminal spine can be longer than the trunk of the animal. For a complete overview of measures and dimensions, see Table 1. The distribution of cuticular structures such as sensory spots and acicular and cuspidate spines is summarized in Table 2. Sensory spots belong to type 1.
The head consists of a long retractable mouth cone and an introvert with five rings of scalids (Figures 3 and 4C-G). The exact position of the inner oral styles could not be examined, but their presence was observed in several specimens. The mouth cone is surrounded by nine anteriorly directed outer oral styles of equal size, composed of two units (Figure 4C,D). The outer oral styles alternate in length and are arranged in a way so that each style is located centrally and anterior to each introvert sector (Figure 4C), except sector 6 where the outer oral style is missing. The anterior parts of the styles point inwards (Figure 4D). The base of each style is characterized by a fringe of small anteriorly directed spines (Figure 4D). Triangular cuticular thickenings are present in between the bases of the oral styles (Figure 4D). The proximal part of the mouth cone, posterior to the outer oral styles, forms a long tube. The tube appears to have longitudinal areas with thickened cuticle and a smooth surface, which alternate with thinner and probably more flexible cuticular areas.
The heads were everted in several paratypes mounted for SEM, but it was often difficult to examine the precise arrangement of scalids; hence, information cannot be provided for all introvert sectors. However, since the kinorhynch introvert usually follows certain symmetry patterns, and information only was missing for three sectors (sectors 1, 2, and 9), we have tried to predict the expected scalid arrangements in these sectors as well. It should be stressed though that the following description is based on incomplete data. The complete polar projection, showing mouth cone and introvert appendages, is shown in Figure 3. Structures in black are based on actual observations, whereas structures in gray are predictions.
The introvert shows spinoscalids in rings 01 and 03 to 06 and trichoscalids in ring 08, whereas ring 02 shows groups of short fringes instead of spinoscalids and ring 03 has both fringes and spinoscalids. The ten primary spinoscalids in ring 01 have three stiff spines on the base, oriented in a way that makes them stick out from the head opening once the introvert is everted (Figure 4E,G). The spines lay flat on the base of the spinoscalids once the introvert is fully everted (Figure 4F). Ring 02 has no scalids. Instead, a group of short fringes, resembling the fringes that often attach at the basal part of a spinoscalid, is present in each introvert sector (Figure 4F). Ring 03 shows both fully developed spinoscalids (two in each even-numbered sector) and the same kind of fringes as in the preceding ring (two in each odd-numbered sector) (Figure 4F). Ring 04 and the following two rings have only fully developed spinoscalids (Figure 3). Ten spinoscalids, one in each sector, are located in ring 04, whereas ring 05 has 20 spinoscalids, two in each sector, and ring 06 has a single spinoscalid in each odd-numbered sector only, giving a total of five spinoscalids in this ring.
Trunk segment 1 shows no prominent cuticular structures (Figures 4A and 5C). Anteriorly, it fuses directly with the head cuticle, and the neck region is only weakly defined as some cuticular thickenings that could be interpret as strongly reduced placids. The reduced placids show no sign of distal tripartition.
Segment 2 has one large middorsal and a pair of large midlateral sensory spots (Figures 2A, 4A, and 6A). A pair of cuspidate spines and a pair of very minute, flexible acicular spines (length ca. 5 μm from SEM), is located in lateroventral positions near the posterior end of the segment (Figures 2B, 5D, and 6A).
Segment 4 has a middorsal spine that extends to the posterior edge of the following segment (Figure 7A). The spine is flanked by a pair of tiny, paradorsal sensory spots. Considerably larger sensory spots are present in sublateral positions (Figure 6B). Elongated hairless patches stretching over the anterior two thirds of the segment are located in mid- or laterodorsal positions (Figures 2A, 6B, and 7A).
Segment 5 has cuspidate spines in ventrolateral positions (Figure 6B). Hairless patches, similar to those on the preceding segment, are present (Figures 6B and 7A), but otherwise the segment has no conspicuous cuticular structures.
Segment 6 has middorsal spine, flanked by a pair of tiny, paradorsal sensory spots. The middorsal spine extends until the anterior part of segment 8 (Figure 7B). Large sensory spots are present in midlateral positions, elongate hairless patches are slightly dorsal to the sensory spots (Figure 6C). The widths of the hairless patches correspond to the width of the sensory spots but their areas extend almost along the entire segment (Figure 6C).
Segment 7 does not have any significant cuticular structures dorsally (Figure 4A). Large sensory spots are present midlaterally (Figure 6C), and hairless patches are similar in size and shape to those on segment 6, slightly dorsal to the sensory spots (Figure 6C).
Segment 8 has a middorsal spine, flanked by a pair of tiny, paradorsal sensory spots. The middorsal spine extends until the posterior edge of segment 9 (Figures 2A and 7C). Acicular spines are present in lateroventral positions and cuspidate spines in lateral accessory positions (Figures 2B, 6D, and 7D). A small, spiny protrusion is present on the cuticular edge of the insertion point of each cuspidate spine (Figure 6D). Lateral sensory spots are not present, whereas hairless patches appear as on the preceding segment.
Segment 9 has a middorsal spine, flanked by a pair of tiny, paradorsal sensory spots. The middorsal spine extends until the posterior edge of segment 10 (Figure 7E). Cuspidate spines are present in lateroventral positions near the posterior edge of the segment (Figure 2A). Large sensory spots are found sublaterally starting in the center of the segment and extending posteriorly, approximately one quarter of the segment (Figure 6D). Hairless patches are present midlaterally extending over 50% of the segment longitudinally (Figure 6D).
Segment 10 tapers slightly towards the posterior and has a middorsal spine that attaches close to the posterior margin of the segment (Figures 2A, 4A, and 7F). It was not possible to determine whether the spine is flanked by paradorsal sensory spots. Additional spines are present in midlateral positions (Figures 2A-B, 4A, 6E, and 7F). Middorsal and midlateral spines appear as regular acicular spines in females, whereas males have crenulated spines. Large sensory spots are present in subdorsal and lateroventral positions (Figures 2A-B and 6E).
Segment 11 tapers strongly towards the midterminal spine at its posterior end (Figures 2A-B, 4A, 5A-B, 6E, and 7G). Additional spines include a middorsal spine and a pair of lateral terminal and lateral terminal accessory spines (Figures 2A-B, 4A, 5B, and 6E). No paradorsal sensory spots are present around the middorsal or midterminal spines, but a pair of tiny sensory spots is present in ventrolateral positions, almost on the posterior edge of the tegumental plate. Female specimens have a pair of rounded gonopores on the ventral side of the segment (Figure 6E). Each gonopore is a round plate with an anterior slit-like opening and a conspicuous cuticular spike attached near the outer lateral edge of the plate (Figure 6E). The cuticular sculpturing of this segment is different from the other segments. Instead of hairs arranged in longitudinal rows, the cuticular hairs are distributed randomly on the surface (Figures 2A-B, 4A, 6E, and 7F).
Notes on diagnostic features
Through its spine pattern, the new species can easily be distinguished from its four congeners. The single diagnostic trait that separates Zelinkaderes yong sp. nov. from other species of Zelinkaderes is its absence of lateroventral or lateral accessory acicular spines on segment 9. Such a spine is present in all four previously described species. Otherwise, it differs most from Z. submersus that shows cuspidate spines in the lateral series on all segments from segments 4 to 9 (Higgins 1990) and from Z. brightae that has ventrolateral cuspidate spines on segments 4 to 6 (Sørensen et al. 2007). In this part of the trunk (segments 4 to 6), Z. yong sp. nov. only possesses cuspidate spines on segment 5. Z. floridensis shows a closer resemblance to the new species, but besides the differences on segment 9, Z. floridensis is unique among its congeners by the absence of cuspidate spines on segment 2 (Higgins 1990). The cuspidate spines on segment 5 in Z. floridensis are furthermore located more laterally compared to the spines in Zelinkaderes yong sp. nov. The new species shows most resemblance with Zelinkaderes klepali. Except for the lateral accessory acicular spine on segment 9, present in Z. klepali and absent in Z. yong sp. nov., the spine patterns of the two species are identical. Also, the distribution of large sensory spots is identical for the two species. Bauer-Nebelsick (1995) reports the positions of some of them as dorsolateral, but according to the provided illustrations, these sensory spots are pretty much located in midlateral positions as in Z. yong sp. nov. The midlateral position of the sensory spots on segments 2, 6, and 7 in Z. klepali was also confirmed by personal examinations of the type specimens, carried out by the last author during a visit at the Natural History Museum of Vienna some years ago. Unfortunately, these examinations could not clarify whether small sensory spots are located near the attachment points of the middorsal spines, but at least Figure twenty three in Bauer-Nebelsick (1995) shows indications of paradorsal sensory spots around the middorsal spine of segment 4. Confirmation of the existence of additional paradorsal sensory spots would probably require SEM examinations, but the SEM specimens used in the description of Z. klepali are unfortunately no longer available (pers. comm. M. Bright). Based on studies of LM material, paradorsal sensory spots similar or identical to the spots of Z. yong are present on segments 4, 6, 8, and 9 of Z. klepali from the Red Sea (Neuhaus pers. comm.) One remarkable difference regarding sensory spots is the apparent absence of type 3 sensory spots around the base of the midterminal spine in Z. yong sp. nov. Such sensory spots have been documented from both Z. klepali and Z. brightae (Bauer-Nebelsick 1995; Sørensen et al. 2007), and they even appear to be quite common in species of other genera with midterminal spine, e.g., Triodontoderes, Antygomonas, Semnoderes, Sphenoderes, Tubulideres, and Wollunquaderes (see Sørensen 2007; Sørensen et al. 2007, Sørensen et al. 2009, Sørensen et al. 2010c; Sørensen and Rho 2009, Sørensen and Thormar 2010).
Additional systematic and morphological remarks
Zelinkaderes yong sp. nov. fits well into the genus Zelinkaderes, with oral styles consisting of two units, segments 1 and 2 consisting of one closed cuticular ring, segments 3 to 11 with midventral articulation of the tergal plate, middorsal spines on segments 4, 6, and 8 to 11, cuspidate spines on segments 5 and 9, cuspidate spines and acicular spines on segment 8, and a conspicuous longitudinal striation pattern formed by rows of cuticular hairs on segments 1 to 10. However, it differs slightly in the composition of its neck region. When Sørensen and Rho (2009) described Triodontoderes anulap and assigned it to Zelinkaderidae, they also proposed an emended diagnosis for the family. In accordance with observations from T. anulap, Z. brightae, Z. klepali, and perhaps also Z. floridensis, Sørensen and Rho (2009) suggested that the presence of distally tripartite placids in the neck could be a common trait for all species of the family. However, this tripartition could not be confirmed for Z. yong sp. nov. because its placids are so inconspicuous that they can hardly be identified. We see this as a reduction that results from the extremely thin cuticle that is found in Z. yong sp. nov. Strongly reduced (or perhaps absence of) placids in species with thin cuticle are also known from other species, e.g., Cateria sp. (see Figure ‘5.1.9.’ in Neuhaus 2013). Zelinkaderids might be either a highly derived taxon or, as suggested by Higgins 1990, a primitive form, closely resembling the common ancestor of the whole phylum.
The introvert in species of Zelinkaderes differs from most other kinorhynchs, due to its reduced number of spinoscalids. This reduction was already noticed in some of the earliest descriptions (see Higgins 1990; Bauer-Nebelsick 1995). In the description of Z. brightae, Sørensen et al. (2007) added more details to the Zelinkaderes introvert morphology by describing other structures, termed ‘fringes’ and ‘spines’, that apparently were replacing spinoscalids and suggested that these structures marked the positions of spinoscalids. We argue that the fringes and spines are reduced spinoscalids, but they might also represent anlagen of not fully developed spinoscalids. The scalid patterns observed in Z. brightae are very similar with those in Z. yong sp. nov. Actually, it appears that the section-wise arrangement of not only spinoscalids but also these peculiar fringes that could mark the position of reduced spinoscalids is identical in the two species. Furthermore, if we expect that Bauer-Nebelsick (1995) reported only the fully developed spinoscalids, leaving out the fringes, the introvert of Z. klepali would be identical with Z. brightae and Z. yong sp. nov. as well.
The finding of a new species of Zelinkaderes in East Asia extends the distributional range of the genus considerably. Species of the genus are now known from European, African, North American, and East Asian waters, which suggests that the genus basically could be present anywhere in the world and could be considered as cosmopolitan. The new species shows the closest resemblance with Z. brightae, but it would be too premature to suggest an actual sister-taxon relationship.
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We wish to thank Wong-Gi Min and Thomas M. Jespersen for their help collecting the new species and processing the samples. This study was supported by a postdoctoral fellowship awarded to AA by the Carlsberg Foundation grant no. 2011_01_0536, by the project of the Survey of Indigenous Biological Resources of Korea (NIBR no. 2014-02-001) to CYC, and the research program of KIOST with contract number PE99204 to HSR.
The authors declare that they have no competing interests.
AA investigated the specimens, made the figures, and drafted the manuscript. HSR and CYC discovered the new species, collected it at the type locality, and contributed to writing of the manuscript. MVS designed and coordinated the study and helped to draft the manuscript. All authors read and approved on the final manuscript.
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Altenburger, A., Rho, H.S., Chang, C.Y. et al. Zelinkaderes yong sp. nov. from Korea - the first recording of Zelinkaderes (Kinorhyncha: Cyclorhagida) in Asia. Zool. Stud. 54, 25 (2015) doi:10.1186/s40555-014-0103-6