Research Article |
Corresponding author: Mian Huang ( huangmian@lcu.edu.cn ) Academic editor: Alexei Tchesunov
© 2024 Mian Huang, Hongxiu Zhai.
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:
Huang M, Zhai H (2024) Two new species of the genus Halichoanolaimus (Nematoda, Selachinematidae) from the intertidal zone of the Yellow Sea, China. ZooKeys 1208: 259-274. https://doi.org/10.3897/zookeys.1208.124047
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Two new marine nematode species belonging to the genus Halichoanolaimus from the intertidal zone of the Yellow Sea are described. Halichoanolaimus sinensis sp. nov. is characterized by amphideal fovea with 2.5–3.0 turns, 20–27% of corresponding body diameters; spicules curved, middle portion broad, tapering distally, 1.4–1.5 cloacal body diameters long; gubernaculum slender consisting of two detached lateral pieces tapering distally; 10–13 papilliform precloacal supplements in two groups, the posterior three supplements smaller and closer to each other, the remaining supplements larger and widely spaced; tail conico-cylindrical with a half cylindrical portion. The second new species, Halichoanolaimus zhangi sp. nov. is distinct by having lateral differentiation present except in anterior half of pharynx which has even punctations, amphideal fovea with 3.0–3.3 turns, spicules curved, gradually narrowing from proximal to distal end with pointed tip, 7 papilliform precloacal supplements, gradually increasing the spacing distance forward, two rows of subventral conical setae situated at the precloacal region, tail elongated, filiform. An updated key to 30 valid species of Halichoanolaimus is provided.
Biodiversity, free-living marine nematode, Halichoanolaimus sinensis sp. nov., Halichoanolaimus zhangi sp. nov., identification key, taxonomy
The Yellow Sea is located on the edge of the western Pacific Ocean, between the Chinese mainland and the Korean Peninsula. It is a semi-enclosed inland shallow sea basin. Biodiversity surveys and taxonomical studies on nematodes in the Yellow Sea have been carried out in recent years. More than 350 species of nematodes have been identified, of which 105 species were new to science (
The genus Halichoanolaimus was established by
In order to investigate the diversity of free-living nematodes along the coast of the Yellow Sea, China, sediment samples were collected in several intertidal sites in 2008 and 2022 respectively. The meiofauna samples were obtained from the top sediment layer (0–8 cm deep) using a 2.9 cm diameter sawn-off syringe. The samples were fixed with an equal amount of 10% formalin solution.
In the laboratory, samples were stained with 0.1% Rose Bengal for more than 12 hours (
Finally, the specimens were mounted in glycerin on permanent slides. Observation and measurement were carried out using a differential interference contrast microscope (Leica DM 2500) and Leica software of LAS X version 3.3.3. Line drawings were made with the aid of a camera lucida. Type specimens were deposited in the Marine Biological Museum of the Chinese Academy of Sciences, Qingdao.
Abbreviations are as follows: a, the ratio of body length to maximum body diameter; abd, body diameter at cloaca or anus; b, ratio of body length to pharynx length; c, ratio of body length to tail length; cbd, corresponding body diameter; c′, ratio of tail length to cloacal or anus body diameter; V%, position of vulva from anterior end expressed as a percentage of total body length.
Class Chromadorea Inglis, 1983
Order Chromadorida Chitwood, 1933
Family Selachinematidae Cobb, 1915
(modified from
Halichoanolaimus anisospermus Leduc & Zhao, 2016
Halichoanolaimus balochiensis Turpeenniemi, Nasira & Maqbool, 2001
Halichoanolaimus bispirae Daschenko & Belogurov, 1991
Halichoanolaimus brandtae Zograf, Trebukhova & Pavlyuk, 2015
Halichoanolaimus caucasicus Sergeeva, 1973
Halichoanolaimus chordiurus Gerlach, 1955
Halichoanolaimus consimilis Allgén, 1933
Halichoanolaimus dolichurus Ssaweljev, 1912
Halichoanolaimus duodecimpapillatus Timm, 1954
Halichoanolaimus funestus Leduc, 2020
Halichoanolaimus lanceolatus Vitiello, 1970
Halichoanolaimus lukjanovae Sergeeva, 1973
Halichoanolaimus macrophallus Gourbault & Vincx, 1985
Halichoanolaimus macrospiculatus Hopper, 1961
Halichoanolaimus minor Ssaweljev, 1912
Halichoanolaimus minutissimus Timm, 1961
Halichoanolaimus norvegicus Allgén, 1940
Halichoanolaimus ossilagulus Leduc, 2020
Halichoanolaimus ovalis Ditlevsen, 1921
Halichoanolaimus possjetiensis Belogurov & Fadeeva, 1980
Halichoanolaimus pumilus Leduc, 2020
Halichoanolaimus quattuordecimpapillatus Chitwood, 1951
Halichoanolaimus raritanensis Hasbrouck, 1966
Halichoanolaimus robustus (Bastian, 1865) de Man, 1886
Halichoanolaimus sicaoensis Xiao & Guo, 2023
Halichoanolaimus sonorus Belogurov & Fadeeva, 1980
Halichoanolaimus stagnalis Gagarin & Long, 2017
Halichoanolaimus unicus Inglis, 1968
Four males and two females were obtained. Holotype: ♂1 on slide RZ08-7-5; paratypes: ♂2 on slide RZ08-7-2, ♂3 on slide RZ08-7-5, ♂4 and ♀1 on slide RZ08-7-3, and ♀2 on slide RZ08-7-2. Type specimens were deposited in the Marine Biological Museum of the Chinese Academy of Sciences, Qingdao.
Holotype and all additional specimens were found from intertidal silt sediment at Rizhao coast of the Yellow Sea; 35°26'N, 119°34'E; 0–2 cm and 2–5 cm sediment depth.
The specific epithet refers to the country origin, China.
All measurement data are given in Table
Individual measurements of Halichoanolaimus sinensis sp. nov. (in µm except for ratios; -, null).
Characters | Holotype | Paratypes | |
---|---|---|---|
male | males (N = 3) | females (N= 2) | |
Total body length | 2416 | 2197±59.0 (2138–2259) | 2792±38.2 (2765–2819) |
Maximum body diameter | 66 | 72.3±2.1(70–74) | 86.0±5.7 (82–90) |
Head diameter | 36 | 35.3±3.1 (32–38) | 39.0±0.8 (37–41) |
Length of outer labial sensilla | 4 | 3.0±0 (3–3) | 3.0±0.0 (3–3) |
Depth of buccal cavity | 46 | 36.0±2.6 (31–38) | 40.0±0.0 (40–40) |
Width of amphid | 14 | 11.3±1.2 (10–12) | 10.0±0.0 (10–10) |
Amphid from anterior end | 20 | 20.0±1.7 (19–22) | 14.0±1.4 (13–15) |
Nerve ring from anterior end | 140 | 117±0 (117–117) | – |
Length of pharynx | 320 | 301.3±24.0 (274–319) | 307.0±18.4 (294–320) |
Body diameter at pharyngeal base | 66 | 67.0±4.0 (63–71) | 69.0±9.9 (62–76) |
Spicule length along arc | 82 | 79.7±5.5 (76–86) | – |
Length of gubernaculum | 42 | 45.0±5.3 (41–51) | – |
Number of precloacal supplements | 10 | 12.0±1.0 (11–13) | – |
Vulva from anterior end | – | – | 1251.5±153.4 (1143–1360) |
V% | – | – | 44.8±4.9 (41.3–48.2) |
Body diameter at cloaca | 55 | 55.3±1.2 (54–56) | – |
Tail length | 166 | 190.7±7.6 (182–196) | 204.0±2.8 (202–206) |
a | 36.6 | 30.4±1.3 (28.9–31.4) | 32.6±2.6 (30.7–34.4) |
b | 7.6 | 7.3±0.8 (6.9–8.2) | 9.1±0.4 (8.8–9.4) |
c | 14.6 | 11.5±0.8 (10.9–12.4) | 13.7±0.0 (13.7–13.7) |
c′ | 3.0 | 3.5±0.2 (3.3–3.6) | 3.1±0.4 (2.8–3.4) |
Males. Body cylindrical, tapering slightly towards posterior end. Cuticle with transverse rows of punctations, lateral differentiation consisting of slightly larger and more widely spaced punctations. Cuticle pore not observed. Somatic setae short, 3 µm long, sparsely distributed. Lip region slightly rounded. Six inner labial sensilla papillose; six outer labial sensilla setiform, 3–4 µm long, at same level as four papilliform cephalic sensilla (Fig.
Microscopic images of Halichoanolaimus sinensis sp. nov. A anterior end of holotype, showing buccal cavity and excretory ampulla (arrow) B anterior end of male 2, showing amphidial fovea C anterior end of holotype, showing stomatorhabdions and anterior sensilla (arrow) D posterior part of holotype, showing supplements E cloacal region, showing spicules, gubernaculum and supplements. Scale bars: 20 μm (A, B, C, E); 30 μm (D).
Reproductive system diorchic with two opposed, outstretched testes. Anterior testis to the right or ventrally to intestine, posterior testis to the left side of intestine. Spicules paired, curved, middle portion broad, tapering distally, 1.4–1.5 cloacal body diameters long, interior of spicules granular in appearance. Gubernaculum slender, consisting of two detached lateral pieces tapering distally, adjoining the dorsal side of spicules. 10–13 papilliform precloacal supplements in two groups, the posterior three supplements smaller and closer to each other (Fig.
Females. Similar to males, but with slightly larger body and slightly smaller amphideal fovea (20% of corresponding body diameter in width and with 2.5 turns). Reproductive system didelphic, with two opposed, reflexed ovaries. Anterior ovary to the left of intestine and posterior ovary to the right of intestine. Vulva situated slightly pre-median. Intestine blind, anus not observed.
Halichoanolaimus sinensis sp. nov. is characterized by amphideal fovea with 2.5–3.0 turns, 20–27% of corresponding body diameter; spicules curved, middle portion broad, tapering distally, 1.4–1.5 cloacal body diameters long; gubernaculum slender consisting of two detached lateral pieces tapering distally; 10–13 papilliform precloacal supplements in two groups, the posterior three supplements smaller and closer to each other, remaining supplements larger and widely spaced; tail conico-cylindrical with half cylindrical portion. The new species is most similar to H. sonorus Belogurov & Fadeeva, 1980 in body shape and number of precloacal supplements, but differs from the latter species by numbers of amphid turns (2.5–3 vs 4–4.2), different shape and structure of spicules (spicules without capitulum, distal hook and central spacer vs with weak capitulum, distal hook and central spacer). The new species is also similar to H. stagnalis Gagarin & Long, 2017 in the number of the amphidial turns and tail, but can easily be distinguished from the latter by the different arrangement of precloacal supplements (3 posterior supplements smaller and closer vs 5–6 smaller and closer supplements
Two males and one juvenile were obtained. Holotype: ♂1 on slide 22HSB-11-2-1; paratypes: ♂2 and juvenile on slide 22HSB-11-2-2. Type specimens were deposited in the Marine Biological Museum of the Chinese Academy of Sciences, Qingdao.
Holotype and paratypes were found from intertidal muddy sediment at Rizhao coast along the Yellow Sea; 35°18'N, 119°31'E; 0–2 cm sediment depth.
The specific epithet “zhangi” is in honor of Professor Zhinan Zhang, a Chinese nematologist, in recognition of his contributions to nematode taxonomy.
All measurement data are given in Table
Individual measurements of Halichoanolaimus zhangi sp. nov. (in µm except for ratios; -, null).
Characters | Holotype | Paratypes | |
---|---|---|---|
♂1 | ♂2 | Juvenile | |
Total body length | 3090 | 3075 | 1940 |
Maximum body diameter | 80 | 79 | 62 |
Head diameter | 63 | 60 | 35 |
Length of cephalic sensilla | 5 | 4 | 5 |
Depth of buccal cavity | 43 | 45 | 32 |
Width of buccal cavity | 32 | 31 | 22 |
Width of amphid | 20 | 18 | 12 |
Amphid from anterior end | 27 | 28 | 21 |
Length of pharynx | 483 | 474 | 332 |
Body diameter at pharyngeal base | 78 | 76 | 60 |
Spicule length along arc | 115 | 106 | – |
Length of gubernaculum | 42 | 40 | – |
Number of precloacal supplements | 7 | 7 | – |
Body diameter at cloaca | 58 | 52 | – |
Tail length | 630 | 590 | 314 |
a | 38.6 | 38.9 | 31.3 |
b | 6.4 | 6.5 | 5.8 |
c | 4.9 | 5.2 | 6.2 |
c′ | 10.9 | 11.3 | 9.2 |
Males. Body cylindrical, tapering slightly towards posterior end. Cuticle with transverse rows of punctations. Lateral differentiation presents except to anterior half of pharynx with even punctations. Lateral differentiation consisting of slightly larger and more widely spaced punctations. Four longitudinal rows of pore complexes situated at sublateral sides of pharyngeal region (Fig.
Microscopic images of Halichoanolaimus zhangi sp. nov. A anterior end of holotype, showing buccal cavity and excretory pore (arrow) B anterior end of holotype, showing cephalic seta (arrow 1) amphidial fovea and cuticle pores (arrow 2) C posterior portion of male 2, showing spicules and tail D cloacal region of holotype, showing spicules, gubernaculum and supplements. Scale bars: 20 μm (A, B, D); 50 μm (C).
Reproductive system diorchic with two opposed, outstretched testes. Anterior testis to the right or ventrally to intestine, posterior testis to the left side of intestine. Spicules paired, curved, gradually narrowing from proximal to distal end with pointed tip, ca 2 cloacal body diameters long. Gubernaculum rod-like, adjoining to the dorsal side of spicules. 7 papilliform precloacal supplements, the most posterior supplement located 14 µm from the cloaca; remaining supplements gradually increasing the spacing distance forward, from 9 µm to 26 µm to each other. Each supplement consists of conical papilla and an internal duct. Two rows of short conical setae situated at two subventral sides of the precloacal supplements region of body. Tail conical with a long posterior filiform portion, accounts for 92% total tail length. A row of 5 caudal setae distributed at ventral side of tail conical part, 3–4 µm long. Caudal glands and spinneret present, 7 µm long.
Microscopic images of Halichoanolaimus zhangi sp. nov. A anterior end of holotype, showing lateral differentiation and somatic setae (arrow) B cloacal region of holotype, showing lateral differentiation and conical setae situated at two subventral sides of precloacal supplements (arrow) C anterior end of juvenile, showing buccal cavity and cephalic sensilla (arrow) D posterior portion of juvenile, showing the end of intestine (arrow). Scale bars: 20 μm (A, B, C, D).
Female not found. Juvenile similar to males in body shape, and with a long filiform tail, except body size smaller, intestine with blind end.
Halichoanolaimus zhangi sp. nov. is distinct by lateral differentiation presenting posterior to the middle of the pharynx, amphideal fovea with 3.0–3.3 turns, spicules curved, gradually narrowing from proximal to distal end with pointed tip, 7 papilliform precloacal supplements, gradually increasing the spacing distance forward, two rows of subventral stout setae situated at precloacal region, tail elongated, filiform. The new species is most similar to H. possjetiensis Belogurov & Fadeeva, 1980 in the filiform tail and number of precloacal supplements, but differs from the latter species by body slender (a=38.6–38.9 vs body stout, a=25.8–26.6), longer tail (c=4.9–5.2 vs c=8–8.3) and different gubernaculum (slender and straight vs. broad and hooked proximally in H. possjetiensis).
1 | Tail consists of anterior conical and posterior filiform parts | 2 |
– | Tail with conical or finger-shaped (not filiform) posterior part | 25 |
2 | Index F (ratio of the filiform portion to the total tail length) ≤ 75% | 3 |
– | Index F ≥ 80% | 16 |
3 | More than 5 amphid turns | 4 |
– | Equal to or less than 5 amphid turns | 7 |
4 | 5.5 amphid turns, 4 precloacal supplements | H. macrophallus |
– | 6.0–6.5 amphid turns, 3 or 5 precloacal supplements | 5 |
5 | 5 precloacal supplements | H. brandtae |
– | 3 precloacal supplements | 6 |
6 | 6.0 amphid turns, index c′ > 5.2 | H. anisospermus |
– | 6.5 amphid turns, index c′=4.7 | H. pumilus |
7 | 4.5–5.0 amphid turns | 8 |
– | 3.0–4.2 amphid turns | 11 |
8 | 6–8 supplements | 9 |
– | 2–4 supplements | 10 |
9 | c′=3.6, spicules 60 µm long | H. ovalis |
– | c′=5.1–6.3, spicules 97 µm long | H. funestus |
10 | c′=3.7–5.2, spicules 43 µm long | H. consimilis |
– | c′=2.4–3.2, spicules 56–59 µm long | H. ossilagulus |
11 | 3–6 posterior-most precloacal supplements smaller and closer to each other than remaining supplements | 12 |
– | All precloacal supplements almost equal in size | 14 |
12 | 3.5–3.8 amphid turns, tail with 3/4 cylindrical portion | H. sicaoensis |
– | 2–3 amphid turns, tail with 1/2–2/3 cylindrical portion | 13 |
13 | Posterior 5–6 supplements smaller and closer, spicules 72–74 µm | H. stagnalis |
– | Posterior 3 supplements smaller and closer, spicules 76–86 µm | H. sinensis sp. nov. |
14 | Amphid with 3.2 turns, 13 supplements, spicules 73 µm long | H. unicus |
– | Amphid with 3.5–4.2 turns, 11–12 supplements | 15 |
15 | Spicules 83–100 µm, 12 supplements | H. duodecimpapillatus |
– | Spicules 63–75 µm, 11 supplements | H. sonorus |
16 | Index c = 3, male body less than 1 mm, supplements and stoma arm absent, spicules 20 µm long | H. minutissimus |
– | Index c > 3, males body longer than 1 mm, supplements present, stoma armed, spicules longer than 40 µm | 17 |
17 | Index c > 14, amphid with 1.5–2.0 turns | H. raritanensis |
– | Index c < 10, amphid with 2–7 turns | 18 |
18 | Dotted denticles posterior to comb in stomatorhabdion, spicules longer than 90 µm | 19 |
– | Dotted denticles absent, spicules shorter than 90 µm | 21 |
19 | Buccal cavity armed with comb consisting of 10 denticles, 5 precloacal papillae | H. balochiensis |
– | Buccal cavity armed with comb consisting of more than 20 denticles, 7 precloacal papillae | 20 |
20 | Body stout, a=26–27, c=8 | H. possjetiensis |
– | Body slender, a=39, c=5 | H. zhangi sp. nov. |
21 | Amphidial fovea 40–50% cbd, precloacal supplements barely visible | H. minor |
– | Amphidial fovea less than 33% cbd, precloacal supplements prominent | 22 |
22 | Comb of each stomatorabdion armed with 7 denticles | H. lanceolatus |
– | Comb of each stomatrhabdion armed with 9–15 denticles | 23 |
23 | Spicules 48–56 µm long, 6–9 precloacal supplements | H. dolichurus |
– | Spicules longer than 70 µm | 24 |
24 | Index F = 96%, 4 precloacal supplements | H. chordiurus |
– | Index F < 96%, 11–14 precloacal supplements | H. quattuordecimpapillatus |
25 | Tail with finger-shaped posterior part | H. macrospiculatus |
– | Tail conical | 26 |
26 | Amphidial fovea 60% cbd, with 6 turns | H. norvegicus |
– | Amphidial fovea more than 60% cbd, more or fewer than 6 turns | 27 |
27 | Index c = 13, spicules 29 µm long | H. robustus |
– | Index c ≥ 16, spicules 50 µm or longer | 28 |
28 | Index c = 17, 2 supplements, spicules 50 µm long | H. caucasicus |
– | Index c = 18–24, 5–14 supplements spicules 76–78 µm long | 29 |
29 | 5 supplements, spicules not cephalated, with groove in the posterior third | H. lukjanovae |
– | 13–14 supplements, spicules cephalated, without groove | H. bispirae |
The authors are very thankful to Wen Guo for her kind help in sample collection. We are sincerely grateful to two anonymous referees for reviewing and improving the manuscript.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This research was funded by the Natural Science Foundation of Shandong Province (grant number ZR2022QC218).
Project Management, work program, methodology and taxonomy: M.H.; experiment, data collection: H. Z.; writing and editing of paper: M.H. All authors have read and agreed to the submitted version of the manuscript.
Mian Huang https://orcid.org/0000-0003-3343-1520
Hongxiu Zhai https://orcid.org/0000-0003-0003-9549
All of the data that support the findings of this study are available in the main text.