Research Article |
Corresponding author: Shinta Fujimoto ( shinta.f@water-bears.com ) Academic editor: Sandra McInnes
© 2015 Shinta Fujimoto.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Fujimoto S (2015) Halechiniscidae (Heterotardigrada, Arthrotardigrada) of Oura Bay, Okinawajima, Ryukyu Islands, with descriptions of three new species. ZooKeys 483: 149-166. https://doi.org/10.3897/zookeys.483.8936
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Marine tardigrades of the family Halechiniscidae (Heterotardigrada: Arthrotardigrada) are reported from Oura Bay, Okinawajima, one of the Ryukyu Islands, Japan, including Dipodarctus sp., Florarctus wunai sp. n., Halechiniscus churakaagii sp. n., Halechiniscus yanakaagii sp. n. and Styraconyx sp. The attributes distinguishing Florarctus wunai sp. n. from its congeners is a combination of two characters, the smooth dorsal cuticle and two small projections of the caudal alae caestus. Halechiniscus churakaagii sp. n. is differentiated from its congeners by the combination of two characters, the robust cephalic cirrophores and the scapular processes with flat oval tips, while Halechiniscus yanakaagii sp. n. can be identified by the laterally protruded arched double processes with acute tips situated dorsally at the level of leg I. A list of marine tardigrades reported from the Ryukyu Islands is provided.
Meiobenthos, northwestern Pacific, subtidal, subtropic, Tardigrada , taxonomy
Halechiniscidae (Heterotardigrada: Arthrotardigrada) is a group of unarmoured marine tardigrades possessing cephalic appendages, including the median cirrus, and legs with four digits terminating in distal claws. More than half of the described marine species are assigned to this family, which comprises 29 genera in seven subfamilies.
In January 2014, the first Umisawa-kai (Field Workshop for Young Marine Biologists) was held to survey the invertebrate fauna of Oura Bay, Okinawajima, one of the Ryukyu Islands, Japan. During this survey, the following five species of Halechiniscidae were encountered: Dipodarctus sp., Florarctus wunai sp. n., Halechiniscus churakaagii sp. n., Halechiniscus yanakaagii sp. n. and Styraconyx sp.
Specimens were found in five sediment samples (each sample was approximately 1L in volume) collected from Oura Bay, Okinawajima, one of the Ryukyu Islands, Japan by SCUBA diving. The geographical coordinates, water depth, sediment type and date of collection are listed for each sediment sample in Table
Sediment sample number | Dive site | Geographical coordinates of dive site | Water depth | Sediment type | Date | Species collected (Number of specimens) |
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1 | Off Sedake | 26°32'39.06"N, 128°2'52.8"E | 6 m | Coarse sand | 24th Jan. 2014 | Halechiniscus churakaagii sp. n. (1) |
2 | Off Camp Schwab | 26°31'51.78"N, 128°3'10.74"E | 9 m | Coarse sand | 25th Jan. 2014 | Florarctus wunai sp. n. (2) |
3 | Off Camp Schwab | 26°31'51.78"N, 128°3'10.74"E | 6 m | Coarse sand | 25th Jan. 2014 | F. wunai sp. n. (2) |
4 | Off Futami | 26°32'42.47"N, 128°2'26.34"E | 6 m | Muddy sand | 27th Jan. 2014 |
Dipodarctus sp. (2) H. churakaagii sp. n. (1) Styraconyx sp. (2) |
5 | Off Thima | 26°32'0.81"N, 128°3'49.61"E | 6 m | Coarse sand | 28th Jan. 2014 |
F. wunai sp. n. (1) H. yanakaagii sp. n. (1) |
The samples were freshwater-shocked (
Two four-clawed juveniles found in sediment sample 4 (Table
The species resembles Dipodarctus borrori Pollock, 1995 and D. susannae Jørgensen, Boesgaard, Møbjerg & Kristensen, 2014 by having digits of unequal length on legs I–III and the lack of lateral processes between legs III and IV. It is distinguished from the two species by the lateral cirrus lack of scapus, which is present in the both D. borrori and D. susannae. It is also distinguished from D. borrori by the shorter digit 1 of legs I–III and from D. susannae by its shorter papillate leg IV sense organ. These observations are based on comparing juveniles with descriptions of adults so while this species is probably an undescribed species observation of an adult specimen is required for confirmation.
Florarctus with smooth dorsal cuticle; six alae with continuous caestus; frontal ala with no caestus; antero-lateral alae caestus with small projection at levels of leg I and II and developed projection at posterior end; postero-lateral alae caestus with parallelogram-shaped projection at posterior end; caudal ala divided into four lobes; caudal alae caestus with pair of small projections; longitudinally elongate secondary clava with internally directed weak swelling.
Holotype: KUZ Z705: adult female found in sediment sample 3 (Table
Paratypes: KUZ Z706: adult female found in sediment sample 2 (Table
Water depth of 6 m, off Camp Schwab, Oura Bay, Okinawajima, one of the Ryukyu Islands, Japan (26°31'51.78"N, 128°3'10.74"E). Collected by the author on 25th January 2014.
The type series is deposited in the Zoological Collection of Kyoto University (KUZ).
Adult female, body length: 257 μm, excluding alae (Fig.
Drawing of Florarctus wunai sp. n., holotype KUZ Z705. A dorsal view B ventral view of cephalic region. a anus; AL anterolateral ala; C caudal ala; ca caestus; cE cirrus E; ec external cirrus; F frontal ala; g gonopore; ic internal cirrus; lc lateral cirrus; mc median cirrus; mo mouth; pb pharyngeal bulb; pc primary clava; PL postero-lateral ala; sc secondary clava; sr seminal receptacle; s1–4 leg I–IV sense organs.
Phase contrast micrograph of Florarctus wunai sp. n. A dorsal view, holotype KUZ Z705, scale bar = 100 μm B secondary clavae (white arrowhead), holotype KUZ Z705, scale bar = 20 μm C bacterial vesicles (white, hollow arrowhead), paratype KUZ Z709, scale bar = 20 μm D caudal alae caestus with pair of small projections (black arrowhead), paratype KUZ Z708, scale bar = 20 μm.
The specific epithet, wunai, is a Ryukyuan word for “sister” (
The adult male, KUZ Z707, was smaller than adult females, KUZ Z705 and Z706, but had longer primary clavae relative to its body length (Table
Morphometrics of the three new species (measurements in μm). Dashes indicate unmeasured trait.
Species | Florarctus wunai sp. n. | Halechiniscus churakaagii sp. n. | Halechiniscus yanakaagii sp. n. | |||||
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Holotype | Paratype | Paratype | Paratype | Paratype | Holotype | Paratype | Holotype | |
KUZ No. | Z705 | Z706 | Z707 | Z708 | Z709 | Z710 | Z711 | Z712 |
Status | Female | Female | Male | ? | Four-clawed juvenile | Female | Female | Female |
Body length | 257 | 241 | 125 | 132 | 122 | 170 | 183 | 170 |
Median cirrus | 36 | 34 | 22 | 19 | 19 | 66 | - | 35 |
Internal cirrus | 46 | 49 | 32 | 29 | 24 | 37 | 40 | 26 |
External cirrus | 44 | 42 | 32 | 28 | 19 | 23 | 24 | 18 |
Lateral cirrus | 43 | 46 | 32 | - | 32 | 68 | 52 | 41 |
Primary clava | 101 | 101 | 78 | - | - | 34 | 38 | 21 |
Cirrus E | 46 | 54 | 37 | 36 | 39 | 86 | - | 41 |
Leg I sense organ | 29 | 31 | 19 | 18 | 14 | 11 | 12 | 14 |
Leg II sense organ | 28 | 29 | 14 | 16 | 12 | 36 | 36 | 21 |
Leg III sense organ | 24 | 28 | 15 | - | 17 | 32 | 33 | 21 |
Leg IV sense organ | 29 | 25 | 17 | 17 | 15 | 16 | 17 | 15 |
Scapular process | absent | absent | absent | absent | absent | 42 | 44 | absent |
Double process (anterior) | absent | absent | absent | absent | absent | absent | absent | 23 |
Double process (posterior) | absent | absent | absent | absent | absent | absent | absent | 26 |
The presence of the continuous caestus and the absence of dorsal mammilla-like ornamentation, are shared by Florarctus antillensis, F. glareolus Noda, 1987, F. pulcher De Zio Grimaldi, Lamarca, D’addabbo Gallo & Pietanza, 1999 and F. wunai sp. n. The new species is distinguished from these three species by the two small projections of the caudal alae caestus, which are long projections in F. glareolus, long projections with swollen tips in F. pulcher and absent in F. antillensis (using
Halechiniscus with cephalic region consisting of antero-medial lobe and dorsal lobe; median cirrus inserted on long robust cirrophore; dorsal internal cirrus inserted on robust cirrophore; ventral external cirrus inserted on short cirrophore; lateral cirrus and primary clava inserted on large lateral cirrophore; large scapular process with flat oval tip; cirrus E with proximal portion with distal dark portion and distal flagellum; bipartite leg I sense organ; large, unsegmented legs II and III sense organs; papillate leg IV sense organ; all claws with calcar.
Holotype: KUZ Z710: adult female found in sediment sample 1 (Table
Paratype: KUZ Z711: adult female found in sediment sample 4 (Table
Water depth of 6 m, off Sedake, Oura Bay, Okinawajima, one of the Ryukyu Islands, Japan (26°32'39.06"N, 128°2'52.8"E). Collected by the author on 24th January 2014.
The type series is deposited in the Zoological Collection of Kyoto University (KUZ).
Adult female, body length: 170 μm (Figs
Drawing of Halechiniscus churakaagii sp. n., holotype KUZ Z710 (dorsal view). a anus; cE cirrus E; d seminal receptacle duct; ec external cirrus; g gonopore; ic internal cirrus; lc lateral cirrus; mc median cirrus; mo mouth; pb pharyngeal bulb; pc primary clava; sc scapular process; s1–4 leg I–IV sense organs.
The specific epithet, churakaagii, is a Ryukyuan word for “beautiful woman” (
The robust cirrophores of the median and lateral cirri are present in Halechiniscus chafarinensis De Zio Grimaldi & Villora Moreno, 1995, H. macrocephalus Grimaldi de Zio, D’Addabbo Gallo & Morone De Lucia, 1988, H. paratuleari Grimaldi de Zio, D’Addabbo Gallo & Morone De Lucia, 1988, H. tuleari Renaud-Mornant, 1979 and H. churakaagii sp. n. Among these species, H. paratuleari and the new species are the only species with large scapular processes. The new species is distinguished from H. paratuleari by the flat oval tip of the scapular process, which is acute in the latter and by the dark portion on cirrus E, which is absent in the latter.
I have interpreted the dorsally positioned cirrus as internal cirrus and the ventrally positioned cirrus as external cirrus in the new species, which is opposite to the interpretation of these features in the original descriptions of H. tuleari and H. paratuleari.
Halechiniscus with no distinct cephalic lobes; only lateral cirrus and primary clava inserted on cirrophore; laterally protruded arched, double processes with acute tips at level of leg I; unsegmented cirrus E; bipartite leg I sense organ; unsegmented legs II and III sense organs; papillate leg IV sense organ; claws of internal digits with dorsal spur.
Holotype: KUZ Z712: adult female found in sediment sample 5 (Table
Water depth of 6 m, Off Thima, Oura Bay, Okinawajima, one of the Ryukyu Islands, Japan (26°32'0.81"N, 128°3'49.61"E). Collected by the author on 28th January 2014.
The holotype is deposited in the Zoological Collection of Kyoto University (KUZ).
Adult female, body length: 170 μm (Figs
Drawing of Halechiniscus yanakaagii sp. n., holotype KUZ Z712 (dorso-lateral view). cE cirrus E; dp1–2 anterior and posterior double processes; ec external cirrus; g gonopore; ic internal cirrus; lc lateral cirrus; mc median cirrus; mo mouth; pb pharyngeal bulb; pc primary clava; s1–4 leg I–IV sense organs.
The specific epithet, yanakaagii, is a Ryukyuan word for “ugly woman” (
Halechiniscus yanakaagii sp. n. and H. tuleari are the only two Halechiniscus species with double processes at the level of leg I. The new species is distinguished from H. tuleari by the absence of distinct cephalic lobes and robust cephalic cirrophores (which are present in the latter species), the similar length, arched, double processes (23 μm, 26 μm) in contrast with a short, straight, anterior process (holotype female: 8 μm; paratype male: 4 μm) and a long, straight, posterior process (holotype female: 19 μm; paratype male: 10 μm) (see:
One female adult and one four-clawed juvenile found in sediment sample 4 (Table
The individuals found resemble Styraconyx nanoqsunguak Kristensen & Higgins, 1984 by the dorsal ridges (Fig.
With the addition of the three new species and two unidentified species reported in this study, two orders, five families, 15 named and two unidentified genera, 13 named and 14 unidentified species of marine heterotardigrades are known from the Ryukyu Islands (Table
Taxon | Sampling locality | References | |
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Order ARTHROTARDIGRADA | |||
Family Batillipedidae | |||
Batillipes pennaki Marcus, 1946 | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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B. similis Schulz, 1955 | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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Family Halechiniscidae | |||
Dipodarctinae | Dipodarctus borrori Pollock, 1995 | Kuroshima |
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D. sp. | Oura Bay, Okinawajima | This study | |
Florarctinae | Florarctus wunai sp. n. | Oura Bay, Okinawajima | This study |
Florarctus sp. 1 (Originally reported as Actinarctus sp.) | Taketomijima and Okinawajima |
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F. sp. 2 | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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F. sp. 3 | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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Wingstrandarctus sp. | Tsunami, Okinawajima |
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Halechiniscinae | Halechiniscus chafarinensis De Zio Grimaldi & Villora Moreno, 1995 | Kuroshima |
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H. churakaagii sp. n. | Oura Bay, Okinawajima | This study | |
H. yanakaagii sp. n. | Oura Bay, Okinawajima | This study | |
H. sp. 1 | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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H. sp. 2 | Tsunami, Okinawajima |
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Styraconyxinae | Angursa clavifera Noda, 1985 | Tsunami, Okinawajima |
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Raiarctus sp. | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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Styraconyx nanoqsunguak Kristensen & Higgins, 1984 | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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S. sp. | Oura Bay, Okinawajima | This study | |
Tholoarctus natans Kristensen & Renaud-Mornant, 1983 | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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Tanarctinae | Tanarctus sp. | Tsunami, Okinawajima |
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Family Renaudarctidae | |||
Renaudarctus psammocryptus Kristensen & Higgins, 1984 | Kabira, Ishigakijima |
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Gen. (?) sp. | Kabira, Ishigakijima |
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Family Stygarctidae | |||
Stygarctinae | Neostygarctus lovedeluxe Fujimoto & Miyazaki, 2013 | Twin Cave, off Shimojijima |
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Parastygarctus higginsi Renaud-Debyser, 1965 |
Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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Stygarctus sp. | Kabira, Ishigakijima and/or Tsunami, Okinawajima |
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Gen. (?) sp. | Off Kuroshima |
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Order ECHINISCOIDEA | |||
Family Echiniscoididae | |||
Anisonyches sp. | Kabira, Ishigakijima |
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As noted above, at best the identifications are ambiguous, and verifying the identity of the species across published papers is difficult. Nonetheless, the data shows that Ryukyu Islands harbour a rich marine tardigrade fauna. With more research we can expect further species discoveries as many of the islands are unexplored and there are currently only seven species reported for the usually species-rich sub-littoral zone.
The author’s thanks are due to the participants of the first Umisawa-kai, especially the two hosts, Daisuke Uyeno and Hiroshi Yamasaki, and the members of the diving team Snack Snufkin for facilitating the opportunity to survey Oura Bay. Thanks are also due to Tsutomu Hikida for helpful comments on the manuscript. This work was supported by Japan Society for the Promotion of Science Grant-in-Aid for JSPS fellows (Grant No. 25987).