Hubrechtella kimuraorum, Kajihara, 2006

Kajihara, Hiroshi, 2006, Four palaeonemerteans (Nemertea: Anopla) from a tidal flat in middle Honshu, Japan, Zootaxa 1163, pp. 1-47 : 37-47

Hubrechtella kimuraorum sp. nov. ( Figs 20–23 )

Diagnosis

Hubrechtella with a short tail; body­wall musculature without zigzag fibres; proboscis musculature composed of inner circular, middle longitudinal, and outer circular layers, without muscle cross; proboscis epithelium with spherical bodies; mid­dorsal blood vessel penetrating into rhynchocoel; foregut blood lacunar network present, followed by a broad U­shaped lacuna.

Etymology The specific name is after Dr Taeko Kimura, a marine ecologist, and Mr Sho­ichi Kimura, a malacologist, who kindly helped me in field sampling.

Material examined Holotype, ZIHU­3127, male, 1 August 2003, HK coll.: 72 slides, 6­µm serial transverse sections of the body except in the middle portion.

External features

The body is translucent white, about 3 cm long, 0.8 mm wide. The head is more transparent and slightly narrower than the following trunk ( Fig. 20 ); the rhynchodaeum is coneshaped, tapering posteriorly, visible through the body wall in the precerebral region. Active search behaviour, such as that of in Hubrechtella ijimai ( Takakura, 1922) comb. nov., was not observed in the living specimen, which held the head rigid while moving, rather than waving it side to side. There is a short, transparent tail region that contains neither intestine nor gonads; it is shorter than twice the width of its basal portion, ending bluntly.

Body wall, musculature and parenchyma

The ciliated epidermis is 20–30 µm thick in the brain region, thickest (up to 50 µm) in the stomach region, and thinnest posteriorly, about 9–10 µm thick in the intestinal region. The distribution of the four types of the glandular cells is similar to that in Hubrechtella ijimai ( Takakura, 1922) comb. nov.; type 4 cell is similarly absent. E (b) = 0.09, E (i) = 0.03.

The basement membrane is about 3–4 µm thick in the brain and foregut regions and about 1 µm thick in the intestinal region. The morphology of the basement membrane in the pre­cerebral region is the same in Hubrechtella ijimai ( Takakura, 1922) comb. nov. The arrangement of the basement membrane and neuro­fibrous layer also becomes inverted in the anterior intestinal region in this species. A mesh­like structure was not found.

The body­wall musculature comprises outer circular and inner longitudinal muscle layers, about 5 µm and 20 µm thick, respectively, in the foregut region ( Fig. 21 ). Zigzag fibres were not found. The diagonal muscle layer is present but not conspicuous. Isolated radial muscle fibres traverse the lumina of the lateral blood lacunae, connecting the body­ wall longitudinal muscle layer with the buccal/foregut wall. A longitudinal splanchnic muscle layer surrounds the foregut and anterior intestine ( Fig. 21 ). Farther back, the dorsal portion of the splanchnic layer is retained between the intestine and rhynchocoel as a longitudinal muscle plate that terminates anterior to the end of the rhynchocoel.

Parenchymatous connective tissue is scarcely developed.

Proboscis apparatus

The rhynchodaeum is composed of 1) an unciliated epithelium, up to 40 µm thick, containing acidophilic glandular cells, 2) a thin, amorphous neuro­fibrous layer, 3) a thin connective tissue layer, and 4) a delicate outer circular muscle layer. Six nerves from the subepidermal neuro­glandular layer innervate the rhynchodaeum ventrolaterally on each side anterior to the proboscis insertion ( Fig. 22A ). No rhynchodaeal sphincter was found.

The rhynchocoel does not extend to the posterior end of the body and posteriorly is not developed into a muscular sac. Its wall contains an outer circular and an inner longitudinal muscle layer, separate from one another. There is no rhynchocoel caecum.

The proboscis insertion is located pre­cerebrally. The proboscis is differentiated into three regions. The anteriormost region contains an outer glandular layer, a neural layer, a longitudinal muscle coat, a thin circular muscle layer one­fibre thick, and an endothelium ( Fig. 22B ). The main component of the epithelium is acidophilic glandular cells, but there are also a few basophilic types. The second, main region is bilaterally symmetrical. A delicate outer circular muscle layer lies between the neural layer and the longitudinal muscle layer ( Fig. 22C ), but there was no indication of a muscle cross between the inner and outer circular muscle layers. In this region the lumen of the proboscis is T­shaped due to two zones of thickened glandular epithelium. The thickened epithelium basally contains conspicuous spherical acidophilic bodies, up to 10 µm in diameter; on the surface of the epithelium, there are much smaller acidophilic spherules, 2–3 µm in diameter ( Fig. 22C ). The third region contains small acidophilic spherules on the surface of its epithelium ( Fig. 22D ); behind it lies the proboscis retractor muscle.

Alimentary canal

The mouth opens close behind the cerebral sensory organs. The buccal/foregut wall reaches 50–60 µm or more in thickness, and is richly glandular and densely ciliated. It contains about equal numbers of basophilic and acidophilic glandular cells. Posteriorly the wall becomes less ciliated. The intestine contains a few basophils. There are no lateral diverticula.

Blood system

Paired lateral cephalic lacunae meet anteriorly above the rhynchodaeal opening. Each lacuna is pierced by isolated bundles of dorsoventral muscle fibres ( Fig. 22A ). The lacunae extend the full length of the head alongside the rhynchodaeum to enter the cerebral ring, where they meet ventrally and give off a small mid­dorsal branch that enters the rhynchocoel ( Fig. 23A ). The U­shaped lacuna soon divides into two branches just anterior to the mouth. Post­orally, these two lateral lacunae extend alongside the rhynchocoel. At the junction between the foregut and intestine, the lateral lacunae meet ventrally below the alimentary canal to form a spacious U­shaped lacuna ( Fig. 21 ) that extends for about 1.3 mm. Posteriorly, the lacuna is divided into two lateral branches and a mid­ventral branch ( Fig. 23B ), which taper posteriorly and connect with one other to form a fine lacunar network ( Fig. 23C ). Eventually, the network fuses to form a pair of lateral vessels lying ventrolateral to the intestine and extending the remaining length of the body ( Fig. 23D ).

The mid­dorsal vessel runs inside the rhynchocoel wall as a rhynchocoelic villus, reaching the middle portion of the foregut. The mid­dorsal vessel then emerges from the rhynchocoel to lie appressed to the alimentary canal. As in Hubrechtella ijimai ( Takakura, 1922 ) comb. nov., the intestinal wall in the vicinity of the mid­dorsal vessel contains basophilic cells ( Fig. 23E ).

No pseudometameric transverse vessels connecting the lateral and mid­dorsal vessels were found.

Nervous system

The arrangement of the nervous system is almost the same as that of Hubrechtella iji­ mai ( Takakura, 1922) comb. nov. The lateral nerve cord contains a giant fibre on its medial side. The dorsal and ventral commissures are about 20 µm and 40 µm thick, respectively.

Frontal organ and cephalic glands There are no frontal organ or cephalic glands.

Sense organs

A ciliated epidermal indentation lies dorsolaterally on each side of the body; it is 60 µm long in the dorsoventral axis and 50 µm long in the anteroposterial axis. The indentation contains no glandular cells, but has cilia about 10 µm long. A ciliated canal 20 µm in maximum external diameter leads from each epidermal indentation to enter the anterolateral side of the cerebral sensory organ, then extends inside the organ for about 70% of the length of the organ before ending blindly. Each cerebral sensory organ is elliptical in cross section ( Fig. 23A ), 68 µm along the minor axis and 85 µm along the major axis, and 140 µm long. Each sensory organ is innervated from the ventral branch of the posterior end of the dorsal ganglion; the core of nerve fibres in the organ is situated medial to the ciliated canal.

Neither eyes nor lateral sensory organs were found.

Excretory system Not found.

Reproductive system

The single specimen is male. The paired testes are about 130 µm in maximum diameter, arranged in a single row on each side of the body, deeply embedded in the intestinal wall ( Fig. 23D ). The anteriormost testis lies anterior to the hind end of the rhynchocoel. A sperm duct, leading from each testis, opens above the lateral nerve cord.

Systematic remarks

Among the known species of Hubrechtella , Hubrechtella kimuraorum sp. nov. is most similar to Hubrechtella ijimai ( Takakura, 1922) comb. nov. in terms of the internal morphology. Apart from the characters listed in Table 3 , Hubrechtella kimuraorum sp. nov. can be distinguished from Hubrechtella ijimai ( Takakura, 1922) comb. nov. by the absence of the muscle cross between the proboscis inner and outer circular muscle layers; the spacious U­shaped blood lacunar connection below the foregut, before the lacuna branches into a lacunar network; the shape of the head, which is narrower than the trunk in Hubrechtella kimuraorum sp. nov., but wider than the trunk in Hubrechtella ijimai ( Takakura, 1922) comb. nov., and the shape of the tail, which is short in Hubrechtella kimuraorum sp. nov. but long in Hubrechtella ijimai ( Takakura, 1922) comb. nov.

Acknowledgements

I am most grateful to Professor Teruaki Nishikawa for kindly arranging my field trip and offering specimens. Thanks are also due to Dr Taeko Kimura and Mr Sho­ichi Kimura for their support in my field sampling; the staff of the Fisheries Laboratory, Graduate School of Agricultural and Life Sciences, the University of Tokyo, for providing me the laboratory facilities and accommodation during my stay; to Mrs Junko Sato for her assistance in taking the digital photomicrographic images of the slides; to Dr Shin Tochinai for computational assistance; to Mr Andrey V. Grischenko for his help in translating Russian literature; to Dr Frank B. Crandall for bibliographic information; and to Professor Emeritus Ray Gibson and Dr Matthew H. Dick for their comments on an earlier version of the manuscript. This study was partially supported by Grants­in­Aid from the Japan Society for the Promotion of Science (research grant no. 16770059) and Wetlands International Japan.

References

Bergendal, D. (1900 a) Studier öfver nemertiner. I. Callinera bürgeri Bergendal, en representant för ett afvikande slägte bland Paläonemertinerna. Lunds Universitets Årsskrift, 36, 1–47.

Bergendal, D. (1900 b) Till kännedomen om de nordiska Nemertinerna. Öfversigt af Kongliga Vetenskaps­Akademiens Förhandlingar, 57, 581–602.

Bergendal, D. (1900 c) Über ein Paar sehr eigenthümliche nordische Nemertinen. Zoologischer Anzeiger, 23, 313–328.

Bergendal, D. (1901) Studier öfver nemertiner. I. Callinera bürgeri Bergendal, en representant för ett afvikande slägte bland Paläonemertinerna. Lunds Universitets Årsskrift, 37, 49–116.

Bergendal, D. (1902 a) Zur Kenntnis der nordischen Nemertinen. 2. Eine der construierten Urnemertine entsprechende Palaeonemerine aus dem Meere der schwedischen Westküste. Zoologischer Anzeiger, 25, 421–432.

Bergendal, D. (1902 b) Zur Kenntniss der nordischen Nemertinen. Bergens Museums Årbog, 4, 1– 22.

Bergendal, D. (1903) Till kännedomen om de nordiska Nemertinerna. 4. Förteckning öfver vid Sveriges vestkust iakttagna Nemertiner. Arkiv för Zoologi, 1, 85–156.

Bürger, O. (1892) Zur Systematik der Nemertinenfauna des Golfs von Neapel. Nachrichten von der Königlichen Gesellschaft der Wissenschaften und der Georg­Augusts­Universität zu Göttingen, 5, 137–178.

Bürger, O. (1904 a) Nemertini. Das Tierreich, 20, 1–151.

Bürger, O. (1904 b) Nemertinen. Resultats du voyage du S. Y. Belgica en 1897–1899, Zoologie, 1– 10.

Bürger, O. (1897 –1907) Nemertini (Schnurwürmer). In: Bronn, H. G. (Ed.), Klassen und Ordnungen des Tier­Reichs, wissenschaftlich dargestellt in Wort und Bild, Vierter Band, Supplement. C. F. Winterísche Verlagshandlung, Leipzig, viii + 542 pp. [1897: pp. 1–176; 1898: pp. 177– 240; 1899: pp. 241–288; 1903: pp. 289–384; 1905: pp. 385–480; 1907: pp. 481–542]

Cantell, C. ­E. (1969) Morphology, development, and biology of the pilidium larvae (Nemertini) from the Swedish west coast. Zoologiska Bidrag från Uppsala, 38, 61–111.

Cantell, C. ­E. (2001) On the anatomy and taxonomy of Tubulanus lutescens n. sp. (Nemertini) from the west coast of Sweden. Ophelia, 54, 213–221.

Chernyshev, A. V. (1995) On the higher taxa of the phylum Nemertea with the taxonomic review of the subclass Anopla. Zoologicheskii Zhurnal, 74, 7–18. [In Russian with English abstract]

Chernyshev, A. V. (1999) Nemertines of the family Carinomidae (Nemertea, Anopla). 1. Description of Carinoma uschakovi sp. n. and Statolitonemertes sachalinica Korotkevitsch. Zoologicheskii Zhurnal, 78, 1275­1283. [In Russian with English abstract]

Chernyshev, A. V. (2002) A new nemertean, Callinera zhirmunskyi sp. n., from the Pacific coast of Canada and a discussion of the taxonomic status of the family Callineridae. Biologiya Morya, 28, 143–146.

Chernyshev, A. V. (2003) A new species of the genus Hubrechtella (Nemertea, Anopla) from the Sea of Japan and establishment of the family Hubrechtellidae. Biologiya Morya, 29, 368–370. [In Russian with English abstract]

Friedrich, H. (1935 a) Carinina poseidoni n. sp., eine neue Palaeonemertine aus der Nordsee. Zoologischer Anzeiger, 109, 64–72.

Friedrich, H. (1935 b) Studien zur Morphologie, Systematik und Ökologie der Nemertinen der Kieler Bucht. Archiv für Naturgeschichte, N. F., 4, 293–375.

Friedrich, H. (1970) Nemertinen aus Chile. Sarsia, 40, 1–80.

Gibson, R. (1979 a) Nemerteans of the Great Barrier Reef. 1. Anopla Palaeonemertea. Zoological Journal of the Linnean Society, 65, 305–337.

Gibson, R. (1979 b) Hubrechtella malabarensis sp. nov. (Palaeonemertea: Hubrechtidae), a new nemertean from Australia. Zoologischer Anzeiger, 202, 119–131.

Gibson, R. (1994) Nemerteans, Synopses of the British Fauna (New Series), Barnes R S K & Crothers J H (Eds), No. 24 (Second Edition), Field Studies Council, Shrewsbury, 224 pp.

Gibson, R. (1995) Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution. Journal of Natural History, 29, 271–562.

Gibson, R. (1997) New benthic nemerteans from Hong Kong. In: Morton, B (Ed.), The Marine Flora and Fauna of Hong Kong and Southern China IV. Hong Kong University Press, Hong Kong, pp. 9–29.

Gibson, R. (2002) The Invertebrate Fauna of New Zealand: Nemertea (Ribbon Worms), National Institute of Water and Atmospheric Research, Wellington, 87 pp.

Gibson, R. & Sundberg, P. (1999) Six new species of palaeonemerteans (Nemertea) from Hong Kong. Zoological Journal of the Linnean Society, 125, 151–196.

Hubrecht, A. A. W. (1885) The Nemertea. Narrativ of the Cruise of H.M.S. Challenger Expedition, 1, 830–833.

Hubrecht, A. A. W. (1887) Report on the nemertea collected by H.M.S. Challenger during the Years 1873 –76. Reports of the Scientific Results of the Voyage of H.M.S. Challenger 1873–1876, Zoology, 19, 1–150.

Hylbom, R. (1957) Studies on palaeonemerteans of the Gullmar Fiord area (West Coast of Sweden). Arkiv för Zoologi, 10, 539–582.

International Commission on Zoological Nomenclature (1985) International Code of Zoological Nomenclature, Third Edition, International Trust for Zoological Nomenclature, London, 338 pp.

International Commission on Zoological Nomenclature (1988) Opinion 1486, Tubulanus Renier, [1804] and T. polymorphus Renier, [1804] (Nemertea): reinstated and made available. Bulletin of Zoological Nomenclature, 45, 157–158.

International Commission on Zoological Nomenclature (1999) International Code of Zoological Nomenclature, Fourth Edition, International Trust for Zoological Nomenclature, London, 306 pp.

Iwata, F. (1951) Nemerteans in the vicinity of Onomichi. Journal of the Faculty of Science, Hokkaido University, Series 6, Zoology, 10, 135–138.

Iwata, F. (1952) Nemertini from the coasts of Kyusyu. Journal of the Faculty of Science, Hokkaido University, Series 6, Zoology, 11, 126–148.

Iwata, F. (1954 a) The fauna of Akkeshi Bay. XX. Nemertini in Hokkaido. Journal of the Faculty of Science, Hokkaido University, Series 6, Zoology, 12, 1–39.

Iwata, F. (1954 b) Some nemerteans from the coasts of the Kii Peninsula. Publications of the Seto Marine Biological Laboratory, 4, 33–42.

Iwata, F. (1957) Nemerteans from Sagami Bay. Publications from the Akkeshi Marine Biological Station, 7, 1–31.

Joubin, L. (1902) Némertiens. Expéditions scientifiques du ‘Travailleur’ et du ‘Talisman’, 4, 181– 220.

Kajihara, H. (2004) Usamaro Takakura (1867–1944), Japanese pioneer nemertean researcher. Archives of Natural History, 32, 208–213.

Kirsteuer, E. (1967) New marine nemerteans from Nossi Be, Madagascar. Zoologischer Anzeiger, 178, 110–122.

Korotkevich, V. S. (1982) Novuie i redkie vidui nemertin (Nemertini) s yuzhnogo shelfa ostrova sakhalin. Issledovaniya Faunui Morei, 37, 12–26. [In Russian]

Kulikova, V. I. (1984) Novyi vid nemertiny roda Carinina (Palaeonemertini, Tubulanidae) iz belogo morya. Zoologicheskii zhurnal, 63, 1092–1095. [In Russian with English abstract]

McIntosh (1873 –1874) A Monograph of the British Annelids. Part I. The Nemerteans, Ray Society, London, 214 pp. [1873: pp. 1–96, pls I–X; 1874; pp. 97–214, pls XI–XXIII]

Melville, R. V. (1986) Tubulanus Renier, [1804] and T. polymorphus Renier, [1804] (Polychaeta): proposed reinstatement under the plenary powers. Bulletin of Zoological Nomenclature, 43, 112–114.

Müller, G. I. (1965) Carinina heterosoma n. sp. Ľi c”teva consideraĘii asupra genului Carinina (Vermes, Palaeonemertini). Hidrobiologia, 6, 243–257. [In Romanian with German abstract]

Nawitzki, W. (1931) Procarinina remanei. Eine neue Paläonemertine der Kieler Förde. Zoologische Jahrbücher, 54, 159–234.

Rogers, A. D., Gibson, R. & Thorpe, J. P. (1992) A new species of Callinera (Nemertea, Anopla, Palaeonemertea) from the Isle of Man. Zoologica Scripta, 21, 119–128.

Senz, W. (1992) Hubrechtella atypica sp. n. (Nemertini: Palaeonemertini). Zoologischer Anzeiger, 229, 185–190.

Senz, W. (1993) Nemertinen europäischer Küstenbereiche (nebst ergänzenden Angaben zur Anatomie von Apartonemertes albimaculosa Wilfert & Gibson, 1974). Annalen des Naturhistorischen Museums Wien, 94/ 95 B, 47–145.

Senz, W. (1997) Morphologie und klassifikatorische Position einiger anopler Nemertinen (Nemertini: Anopla). Annalen des Naturhistorischen Museums in Wien, 99 B, 423–496.

Senz, W. (2000) Neue Nemertinen aus dem Golf von Arabien. 1. Palaeonemertini. Annalen der Naturhistorischen Museums in Wien, 102 B, 321–373.

Shimomura, M., Kato, T. & Kajihara, H. (2001) Records of some marine invertebrates (nemerteans, asellotes and phyllodocids) from the coast around Otsuchi Bay. Otsuchi Marine Science, 26, 46–50.

Sundberg, P. & Hylbom, R. (1994) Phylogeny of the nemertean subclass Palaeonemertea (Anopla, Nemertea). Cladistics, 10, 347–402.

Sundberg, P., Turbeville, J. M. & Lindh, S. (2001) Phylogenetic relationships among higher nemertean (Nemertea) taxa inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution, 20, 327–334.

Takakura, U. (1898) Misaki kinbousan himomushi (Nemertini) no bunrui [Classification of the nemerteans of the vicinity of Misaki]. Zoological Magazine, Tokyo, 10, 38–44, 116–120, 184– 187, 331– 337, 424–429. [In Japanese]

Takakura, U. (1922) Honpousan himomushi no ichi shinzoku ni tsukite [On a new genus of nemertean from Japan]. Zoological Magazine, Tokyo, 34, 419–422. [In Japanese]

Thollesson, M. & Norenburg, J. L. (2003) Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proceedings of the Royal Society of London, Series B, 270, 407–415.

Wada, M., Sugiura, H., Fujihara, S., Ho, Y., Hosoi, E., Isa, T., Yokoyama, I., Nishibori, C., Hagihara, K. & Kubo, A. (2002) DeltaViewer Project. DeltaViewer Project Team, Department of Information and Computer Sciences, Nara Women’s University, Japan. Available from: http:// vivaldi.ics.nara­wu.ac.jp/˜wada/DeltaViewer/ (accessed 16 September 2005)

Wheeler, J. F. G. (1940) Nemerteans of Kerguelen and the southern ocean. B. A. N. Z. Antarctic Research Expedition Report, Series B, 4, 233–256.

Yamaoka, T. (1940) The fauna of Akkeshi Bay. IX. Nemertini. Journal of the Faculty of Science, Hokkaido Imperial University, Series 6, Zoology, 7, 205–263.

Figures

FIGURE 20. Hubrechtella kimuraorum drawing based on a photograph taken in life to show the general shape of the body.

FIGURE 21. Hubrechtella kimuraorum sp. nov. Holotype, male, ZIHU­3127, drawing of a transverse section through the foregut region showing the well developed lacunar connection below the alimentary canal. BM, basement membrane; DV, mid­dorsal vessel; EP, epidermis; FG, foregut, LM, body­wall longitudinal muscle layer; LN, lateral nerve cord; OC, body­wall outer circular muscle layer; PR, proboscis; UB, U­shaped blood lacuna below gut; UD, upper mid­dorsal nerve.

FIGURE 22. Hubrechtella kimuraorum sp. nov. Holotype, male, ZIHU­3127. A, transverse section through the pre­cerebral region; white arrowhead indicates a dorsoventral muscle fibre in the cephalic lacuna (CL), black arrowheads indicate innervation from the subepidermal neuro­glandular layer to the rhynchodaeum (RD). B, transverse section through the first region of the proboscis. C, transverse section through the second region of the proboscis; arrowhead indicates an acidophilic spherical body. D, transverse section through the third region of the proboscis; arrowheads indicate acidophilic spherules. PE, proboscis epithelium; PI, proboscis inner circular muscle layer; PL, proboscis longitudinal muscle layer; PN, nervous layer of proboscis; PO, proboscis outer circular muscle layer.

FIGURE 23. Hubrechtella kimuraorum sp. nov. Holotype, male, ZIHU­3127. A, transverse section through the cerebral sensory organ (CO). B, transverse section through the foregut region; arrowhead indicates the ventral branch of the lacunar connective. C, transverse section through the foregut region showing the appearance of the lacunar network below the foregut (indicated by the arrowheads). D, transverse section through the intestinal region showing the arrangement of the testes. E, higher magnification of part of D showing basophilic cells (indicated by the arrowhead) in the intestinal wall around the mid­dorsal vessel. CL, cephalic blood lacuna; DV, mid­dorsal vessel; IN, intestine; LL, lateral blood lacuna; LV, lateral blood vessel; PR, proboscis; RM, proboscis retractor muscle; TS, testis.