Zootaxa, A revision of the genus Paranarthrurella ...

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A revision of the genus Paranarthrurella Lang, 1971a (Crustacea: Tanaidacea) PIOTR JÓŹWIAK, ANNA STĘPIEŃ & MAGDALENA BŁAŻEWICZ-PASZKOWYCZ Department of Polar Biology and Oceanobiology, University of Łódź, Banacha 12/16, Łódź 90–237, Poland. E-mail: [email protected]

Abstract The revised genus Paranarthrurella Lang, 1971a includes three species: P. caudata (Kudinova-Pasternak, 1965), the type species of the genus, P. dissimilis (Lang, 1972), and P. voeringi (G.O. Sars, 1877), which were all originally and subsequently classified in other genera (Leptognathia, Cryptocope, Robustognathia and Biarticulata). The genus is defined by a set of specific characters: a long and narrow labrum, a rounded molar, large lacinia mobilis widely separated from incisor; maxillule with eleven spiniform setae distally and numerous simple setae on outer margin; maxilliped with narrow endites and two flat setae on the distal margin; and a chela with well calcified ‘crushing margins’. The genus is most close related to Armatognathia Kudinova-Pasternak, 1987 and it is suggested that both genera may constitute a new family. Key words: Arctic Ocean, Tanaidacea, Cryptocope, Biarticulata, Robustognathia, Agathotanaidae, Anarthruridae

Introduction The genus Paranarthrurella was established by Lang in 1971 for Leptognathia caudata Kudinova-Pasternak, 1965 and primarily classified in the family Anarthruridae Lang, 1971a. It is unclear how Lang (1971a) deduced that the cheliped is attached to the cephalothorax by a pseudocoxa in L. caudata, as no such information was given in the original description. In his discussion Lang (ibid.) mentioned that the genus is an atypical anarthrurid owing to the regular structure of the uropods which are composed of two well-developed rami and they lack the protopod projection that characterizes all members of the Anarthruridae (and also Agathotanaidae Lang, 1971a). Based on the last feature, as well as the pseudocoxa on the chelipeds (sic!), Larsen and Wilson (2002) have classified Paranarthrurella in the Agathotanaidae. The north-eastern Atlantic “Tanais” voeringi was initially described by G.O. Sars (1877, as Tanais Vøringi). G.O. Sars (1882, 1885) subsequently recognized it as member of Cryptocope G.O. Sars, 1882. Complementary descriptions were given by Hansen (1913) and G.O. Sars (1885) but they only concerned some superficial features such as habitus and general structure of the cheliped, pereopods and uropods. Sieg (1983) moved the species into the “catch-all” genus Leptognathia G.O. Sars, 1882. Larsen and Shimomura (2007) erected the genus Biarticulata to accommodate those leptognathid species with a biarticulated exopod of the uropod. That pragmatic and clearly polyphyletic genus incorporated T. voeringi along with eight other species (see Bird 2007). A comprehensive study of recent specimens of T. voeringi collected in Fram Strait (West of Spitsbergen) and of the types loaned from Natural History Museum (University of Oslo) allowed us to deduce T. voeringi and P. caudata belong in the same genus – Paranarthrurella. Two other species that have to be included in Paranarthrurella on account of having the same peculiar mouthparts are: Leptognathia dissimilis Lang, 1972, which was classified to the monotypic genus Robustognathia by Kudinova-Pasternak (1989) and Strongylura arctophylax (Norman & Stebbing 1886) known from only one specimen. The later species was included to Cryptocope by Hansen (1913) and later by Sieg (1983) transferred to genus Leptognathia. In this paper S. arctophylax is synonymized with T. voeringi.

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Accepted by S. Gerken: 26 Aug. 2009; published: 23 Sept. 2009

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Materials and methods The new material studied was collected in Arctic waters from the R/V Polarstern from 16th of June to 16th of July, 2004 in Kongsfjord Canyon and from 10th to 25th of July, 2007 at Hausgarten station. The specimens of P. voeringi were found in the stomachs of the zoarcid fish Lycodes frigidus Collett, 1879 and L. squamiventer Jensen, 1904; additional samples were collected using an Agassiz trawl. The type specimens of “Tanais” voeringi were loaned from the Natural History Museum at the University of Oslo (NHMO F1691a; NHMO F1691b) and Strongylura arctophylax (NHM 1903.5.20.8) loaned from The Natural History Museum in London. The synonymy in the paper is based mostly on Sieg (1983). The morphological terminology follows Larsen (2003) and Bird (2004).

Systematics Suborder Tanaidomorpha Sieg, 1980 Superfamily Paratanaoidea Lang, 1949 Family incertae sedis Genus Paranarthrurella Lang, 1971a Tanais Latreille, 1831 (partim.): G.O. Sars, 1877: 347, 370; G.O. Sars, 1882: 50; G.O. Sars, 1896: 33; Sieg, 1980: 11–12. Cryptocope G.O. Sars, 1882 (partim.): G.O. Sars, 1882: 50–51; G.O. Sars, 1885: 74–78; Forsstrand, 1886: 47; Norman, 1899: 340; Zirwas, 1911: 105; Hansen, 1913: 106, 109–110, pl X; Nierstrasz, 1913: 33; Lang, 1949: 6, 8; Stephensen, 1932: 349; Lang, 1971b: 403. Leptognathia G.O. Sars, 1882 (partim.): Kudinova-Pasternak, 1965: 75, 88–91; Belyaev, 1966: 88; Kudinova-Pasternak, 1968: 73; Lang, 1968: 160–161; Lang, 1971a: 361–362; Gardiner, 1975: 225; Lang, 1972: 229–235; KudinovaPasternak, 1981: 115; Sieg, 1983: 317. Strongylura G.O. Sars, 1882 (partim.): Norman & Stebbing, 1886: 110, 133. Paranarthrurella Lang, 197a1: Lang, 1971a: 361, 363, 367; Sieg, 1973: 34–281; Sieg, 1976: 178; Sieg, 1978: 121. Robustognathia: Kudinova-Pasternak, 1989: 68, 33–34. Biarticulata Larsen & Shimomura, 2007 (partim): Larsen & Shimomura, 2007: 19; Bird, 2007: 75. Gender: Feminine. Type species: Leptognathia caudata Kudinova-Pasternak, 1965; by original designation (Lang, 1971a). Species included: Paranarthrurella caudata; P. (=Leptognathia) dissimilis Lang, 1972; P. (=Tanais) voeringi G.O. Sars, 1877.

Amended diagnosis: Female: antennule with five articles, distal article vestigial. Antenna with six articles. Labrum long and narrow. Mandibular molar rounded distally, with 5–7 short, flat distal setae, incisor large and gently rounded, lacinia mobilis large and widely separated from incisor. Maxillule with eleven spiniform setae distally and numerous simple setae on outer margin; labium strongly setose with poorly-developed outer lobe; maxilliped with narrow endites, bases with small seta distally; endites with pair of simple and pair of short flat setae distally. Epignath distally narrow. Chelipeds usually robust; attached to cephalothorax by sclerite; chela with well calcified ‘crushing margins’. All pereopods of walking type; pereopod-1 setation strongly reduced; pereopods 2–6 with short and robust setae. Pleopods absent or reduced in female. Uropods biramous, both rami 2-articled. Male: swimming type; antennule with seven articles; articles 4–6 with numerous aesthetascs; mouthparts reduced; cheliped and pereopods similar to female; pleopod rami elongated with setulated setae distally; uropod endopod with three, exopod with two articles.

A REVISION OF PARANARTHRURELLA LANG, 1971

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Remarks: The genus Paranarthrurella has a set of very distinctive characters, especially in the morphology of the mouthparts, which exclude it from any of the families recognized by Larsen and Wilson (2002). The systematic position of Paranarthrurella remains unresolved, and it is proposed that the genus becomes family incertae sedis until there is a better understanding of the systematics of the paratanaoid tanaidomorph genera. Paranarthrurella is most closely related to Armatognathia Kudinova-Pasternak, 1987, sharing with it the specific mouthpart morphology which includes an elongated labrum (e.g. Fig. 2C), a setose outer margin of the maxillule (Fig. 2F), and the bizarre shape of the mandibles (Fig. 2D). The mandible incisor is massive and gently rounded; the lacinia mobilis (on the left mandible only) forms a gentle depression that, together with the incisor, forms a spoon-like structure; the mandibular molar in both genera is large, but gently rounded distally, with short simple or blunt spiniform setae. The maxillipeds have quite narrow endites which are of similar width proximally and distally. A peculiar character in the genus is the projection on the inner margin of the cheliped dactylus, that matches a depression on the inner margin of the fixed finger (e.g. Fig. 3A). It is difficult to judge the function of the structure without direction observation or at least information about stomach contents. It can be assumed however, that it is used for crushing the food particles (e.g. forminiferan tests). Females studied by us have an antennule of five articles, although the last article is vestigial. This character has often been overlooked in the past, and is so far confirmed for such genera as Collettea Lang, 1973, Robustochelia Kudinova-Pasternak, 1983 and Tanaopsis G.O. Sars, 1896. The family classification of Paranarthrurella remains uncertain, although it cannot be classified to either the Anarthruridae or the Agathotanaidae. The regular structure of uropods and cheliped attachment to the cephalothorax by a sclerite suggest its relationship to some leptognathids or colletteids. More probable however is that this genus, together with Armatognathia, constitute a new family that may yet be confirmed through phylogenetic analysis.

Key to females of the genus Paranarthrurella 1. 2. -

Cheliped carpus twice as long as wide .......................................................................................................... P. caudata Cheliped carpus as long as wide ................................................................................................................................... 2 Antennule article 1 twice as long as article 4; mandible molar with more than ten short setae distally, pleon without hyposphaenium ............................................................................................................................................ P. dissimilis Antennule article 1 only little longer than article 4; mandible molar with less than seven short setae distally; pleon with three hyposphenia ..................................................................................................................................P. voeringi

Paranarthrurella caudata (Kudinova-Pasternak 1965) Leptognathia caudata: Kudinova-Pasternak, 1965: 81, 88–91, Fig.7. Paranarthrurella caudata: Lang, 1971a: 361–363.

Diagnosis: body slender, 7.3 times as long as wide; antennule article 1 little longer than article 4; mandibular molar with a few (seven or less) flat setae terminally; cheliped carpus twice as long as wide; pleonites 2, 3 and 4 without hyposphenia. Holotype is deposited at Zoological Museum of Moscow S-ZMM Mc938; not accessible for this study. Distribution: The species is known only from its type locality, the Bougaunville Trench (6°13,4' S, 153°43,7' E) at a depth range from 7947 to 8006 m.

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Paranarthrurella dissimilis (Lang, 1972) Leptognathia dissimilis: Lang, 1972: 229–235, figs. 6–9.; Kudinova-Pasternak & Pasternak, 1978: 113, 182, 193. Robustognathia dissimilis: Kudinova-Pasternak, 1989: 68, 33–34.

Diagnosis: antennule article 1 twice longer as article 4; mandibular molar with more than 10 flat setae terminally; cheliped carpus as long as wide; pleonites 2, 3 and 4 without hyposphenia. Holotype is deposited at Zoological Museum University of Copenhagen (ZMUC CRU-6295); not examined in this study. Distribution: The species is known only from its type locality, the Sargasso Sea (26°06' N, 57°32' W) at 6000 m depth.

Paranarthrurella voeringi (G.O. Sars, 1877) (Figures 1–5) Tanais voringi: G.O. Sars, 1877: 2, 347–370. Cryptocope voringii: G.O. Sars, 1882: 7, 50–51; G.O.Sars, 1885: 6, 74–78, pl. VII; Hansen, 1913: 3, 109–110, pl. X. Strongyrula arctophylax: Norman & Stebbing, 1886: 12, 110, 116–117, pl. 24 Fig. III. Cryptocope arctophylax: Hansen, 1913: 3, 106, 110–113, pl. 11 Fig. 2a–k. Leptognathia arctophylax: Sieg, 1983: 317, Lang ,1971b: 403. Tanais voeringi: Sieg, 1980: 537, 11–12. Leptognathia voeringi: Sieg, 1983: 356. Biarticulata voeringi: Larsen & Shimomura, 2007: 19.

Material examined: Cryptocope voringii lectotype female, ((NHMO F1691a), sta. 31, 124, 240, 63°10.2' N, 4°59.6' E, depth 760 m; paralectotypes: two males, ((NHMO F1691b), sta. 31, 124, 240, 63°10.2' N, 4°59.6' E, depth 760 m; Strongylura arctophylax, type, (NHM 1903.5.20.8), 56°24'N, 11°19'W (between Ireland and Rockall) 2524 m. Additional material: four females, PS72/137–5, sta. HG I, 79°7.75' N, 6°7.46' E, depth 1237 m; ten females and one male, PS66/103–1, sta. HGI, 79° 8.97' N, 5° 56.35' E, depth 1300 m. Diagnosis female: body robust, 5.2 times as long as wide; antennule article 1 little longer than article 4; mandibular molar with a few (seven or less) flat setae terminally; cheliped carpus as long as wide; pleonites 2, 3 and 4 with hyposphenia. Male: swimming type; antennule with seven articles; articles 4–6 with numerous aesthetascs; mouthparts reduced; maxilliped as in females, but endites three times as long as wide, setae on palp articles 2–4 much longer than in female; cheliped and pereopods similar to female, inner side of palm with 17 setae; pleopod rami elongated with setulated setae distally; uropod endopod with three, exopod with two articles. Description of female: Body (Figs 1A, B) 5.0 mm long; 5.2 times as long as wide. Carapace 17% of body length, narrowing proximally. Pereonites rounded; pereonite 1 0.4 times as long as wide; pereonite 2 little longer, equal in length to pereonites 3 and 6; pereonites 4 and 5 little longer than pereonite 2; pleon 23% of body length, pleonites 1–5 equal, pleonites 2, 3, and 4 with ventral hyposphenia (Figs 1C, D); pleotelson wider than pleonites, 0.3 times as long as wide, with few simple setae distally. Antennule (Fig. 2A): 5-articled. Article 1 two times as long as wide, with one distal seta on inner margin and one simple and seven bipinnate setae on outer margin. Article 2 over 0.4 times as long as article 1, with two simple and two bipinnate setae distally. Article 3 about half as long as article 2, with one simple and one bipinnate seta distally. Article 4 three times as long as article 3, terminated by one simple and one bippinate seta. Article 5 vestigial, with five setae.



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FIGURE 1. Paranarthrurella voeringi. Female. A) body dorsally; B) body laterally; C) pleon laterally; D) pleon ventrally. Scale bar equals 1 mm.

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FIGURE 2. Paranarthrurella voeringi. Female. A) antennule; B) antenna; C) labrum; D) left mandible; D’) left mandible of paralectotype female; E) right mandible; F) maxillule; F') palp of maxillule; G) labium; H) maxilliped. Scale bars equal 0.1 mm.



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FIGURE 3. Paranarthrurella voeringi. Female. A) cheliped; A’) chela inner side; B) pereopod 1; C) pereopod 2; D) pereopod 3; E) pereopod 4; F) pereopod 5; F’) details of pereopod 5 merus; F”) details of pereopod 5 propodus; G) pereopod 6; H) pleopod; I) uropod. Scale bars equal 0.1 mm

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FIGURE 4. Paranarthrurella voeringi. Male. A) body, dorsally; B) body; laterally. Scale bar equals 1 mm.

Antenna (Fig. 2B): 6-articled; article 1 short, wider than long. Article 2 and article 3 each with simple distal seta. First three articles with microtrichia. Article 4 longest almost twice as long as article 5, with three simple and five bipinnate setae distally. Article 5 two times as long as article 4, with one serrated seta. Last article very short, with two short, simple and three serrated setae terminally. Mouthparts: Labrum (Fig. 2C) long with numerous short setae distally. Mandibles (Figs 2D-E) with proximal inner margin covered by numerous minute setae; molar process short, broad and rounded, distally with six or seven short, massive setae (broken on Fig. 2D); lacinia mobilis well-developed, as long as incisor, A REVISION OF PARANARTHRURELLA LANG, 1971


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strongly crenulated; incisor of left mandible with dorsal row of small denticles. Maxillule (Fig. 2F) with eleven strong spines terminally; outer margin with simple setae; inner margin with rows of minute setae; palp with two setulated setae. Labium (Fig. 2G) bilobed; inner lobe with numerous, short setae along distal and outer margin, inner surface strongly crenulated and calcified; outer lobe, vestigial, each with small tubercle. Maxilliped (Fig. 2H) bases with minute seta distally; endites distally with two simple and two short, flat setae, numerous minute setae on disto-inner margin; palp article 1 naked; article 2 with simple seta on outer margin and long simple and two short setulated setae on inner margin; article 3 with four setulated setae on inner margin and some microtrichia; article 4 with one outer, simple seta, rows of minute setae on inner margin and four setulated setae terminally. Cheliped (Fig. 3A): basis wide, naked; merus 0.7 times as long as carpus, with one simple seta ventrally; carpus 1.3 times as long as propodus, with two simple setae on dorsal and ventral margins. Propodus with row of eleven simple setae on inner surface near dactylus insertion and with numerous minute spines; fixed finger with strong claw, two simple setae ventrally; inner margin with teeth and 3 simple setae (Fig. 3A’). Dactylus with simple seta in middle. Pereopod 1 (Fig. 3B): coxa with seta; basis 6.5 times as long as wide, about 4.3 times as long as merus, naked; ischium with simple seta ventrally; merus 0.5 times as long as carpus, with two simple setae on distoventral margin; carpus subequal in length to propodus, with five simple setae subdistally; propodus as long as combined length of dactylus and unguis, with three simple setae on distal margin and one long seta on inner face; unguis 1.7 times as long as dactylus. Pereopod 2 (Fig. 3C): similar to pereopod 1, but basis with two bipinnate setae dorsally, carpus with three serrated setae distally and propodus with row of short, simple setae distally. Pereopod 3 (Fig. 3D): similar to pereopod 1, but carpus with four serrated setae distally and propodus with row of short, simple setae distally. Pereopod 4 (Fig. 3E): basis 3.6 times as long as merus, with two bipinnate setae ventrally; ischium with two simple setae distoventrally; merus 0.7 times as long as carpus, with two serrated setae on distoventral margin; carpus 0.7 times as long as propodus, with four serrated and one simple setae distally; propodus more slender than carpus, with bipinnate seta and two spines dorsally, three serrated and two short setae; dactylus little longer than unguis; both as long as carpus. Pereopod 5 (Fig. 3F): similar to pereopod 4, but basis with additional bipinnate seta on dorsal margin; merus (Fig. 3F’) with doubly-serrated seta and some microtrichia; propodus (Fig. 3F’’) with doubly-serrated seta and spine on dorsodistal margin. Pereopod 6 (Fig. 3G): similar to pereopod 4, but basis naked; propodus with five serrated setae distally and with some microtrichia. Pleopod (Fig. 3H): basal article about 1.5 times as long as wide; both endopod and exopod with only rudimentary setation (3 short setae terminally). Uropod (Fig. 3I): basal article about as long as wide. Exopod 2-articled; article 1 with one simple seta, article 2 with two simple setae terminally. Endopod 2-articled; article 1 as long as exopod with 2 bippinate setae, article 2 with five simple and two bipinnate setae terminally. Description of male: Body (Figs 4A, B) 4.1 mm long; 6.2 times as long as wide. Carapace about 22% of total body length, tapering distally. Pereonites wider than long, width: length ratios are 2.4, 2.3, 2.4, 1.9, 1.4, 2.0 respectively. Pleon relatively long, 35% of total body length; pleonites equal, 2.2 times as wide as long; pleotelson almost 1.2 times as wide as long, terminating in long and narrow apex; apex bears two simple distal setae. Antennule (Fig. 5A): 7-articled, about 1.5 as long as carapace. Article 1 with two simple and seven bipinnate setae distally and subdistally. Article 2 1.2 times as wide as long with two simple (one long) and three bipinnate setae distally. Article 3 0.4 as long as article 2, with two simple and one bipinnate setae. Articles 4–6 width: length ratios are 2.3, 1.0 and 0.4 respectively; all with dense row of long, simple setae distally. Last article 4.8 times as long as wide, with one bipinnate and six simple setae terminally.

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FIGURE 5. Paranarthrurella voeringi. Male. A) antennule; B) maxilliped; C) cheliped; D) pleopod; E) uropod. Scale bars equal 0.1 mm.



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Maxilliped (Fig. 5B) bases about as long as wide, with simple, short seta distally. Endites narrow and elongated, three times as long as wide, with two simple and two flat setae terminally. Palp article 1 naked; article 2, with three simple setae on inner margin; article 3 with four setae distoventrally; last article terminated by one short and five long, simple setae. Cheliped (Fig. 5C): basis with wide sclerite, bearing one simple subdistal seta. Merus triangular, with one ventral seta. Carpus tapering distally, about 1.5 times as long as wide, with two inner and one outer setae; distally with small tubercle. Propodus about as long as wide, with seventeen simple setae (increasing in length) near dactylus insertion. Fixed finger with two setae ventrally and three on inner margin; inner margin well calcified. Dactylus with one simple seta proximally and process on inner margin near unguis insertion; unguis over one third as long as dactylus. Pereopods 1–6 similar to those of female. Pleopod (Fig. 5D): basal article about 1.5 times as long as wide, naked. Both rami elongate, equal in length. Endopod with thirteen setulated setae (outer setae shorter), proximal seta separated from remainder by gap. Exopod terminating in sixteen setulated setae. Uropod (Fig. 5E): basal article naked. Endopod 3-articled; article 1 with seven bipinnate setae; article 2 with two bipinnate setae; article 3 with five simple and two bipinnate terminal setae. Exopod 2-articled, about 0.6 times as long as endopod; article 1 with distal, simple seta; article 2 little longer than article 1, with two simple terminal setae (one long). Distribution: The recently collected material is from the Fram Strait (north west of the Svalbard Archipelago) from a depth of 1300 m. Previously the species was known from west of Norway from a depth range 630 to 1825 m. Remarks: Of the three species now classified in the genus, Paranarthrurella voeringi is distinguished by its relatively short body, about 5.2 as long as wide, and the well developed hyposphenia on pleonites 2–4. In P. dissimilis and P. caudata the length:width body ratio equals 9.5 and 6.2 respectively while hyposphenia are absent. The first article of the antennule of P. voeringi is relatively short (length:width ratio is 1.6) and it is little longer than the length of the fourth article. The length to width ratio of this article in P. caudata and P. dissimilis is 2.8 and 3.4 respectively. Moreover, P. voeringi has seven simple, flat setae on the mandible molar and eleven simple setae on the inner surface of the cheliped propodus, while in P. dissimilis the molar has eleven short, flat setae and the propodus of the cheliped has only eight setulated setae.

Acknowledgements The examined material was loaned through the courtesy of Dr Melanie Bergmann from the Alfred Wegener Institute for Polar & Marine Research. The authors are grateful to Professor Lutz Bachmann and Åse Ingvild Wilhelmsen (Natural History Museum, University of Oslo) and to Miranda Lowe (Natural History Museum, London) for loan of type material. Dr Roger Bamber kindly corrected English through the manuscript. The research was financed by MNiSW grant 2PO4C 089 29.

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