Liljeborgia associata, Marin, 2020

Marin, Ivan, 2020, A new species of the genus Liljeborgia Spence Bate, 1862 (Crustacea: Amphipoda: Liljeborgiidae) associated with the burrows of the spoon worm Urechis unicinctus in the Sea of Japan, European Journal of Taxonomy 613, pp. 1-19 : 4-14

Liljeborgia associata sp. nov.

urn:lsid:zoobank.org:act:CC2A771F-71B2-4EED-9C16-3EF17CD0655D

Figs 1 – 5

Diagnosis

A1 with stout articles 2 (about as long as wide) and 3 (about 1.5 times as long as wide), article 2 with dorsal projection produced into a rounded lobe; palp of Md with long and slender articles, article 3 almost equal to articles 1 and 2, about 5 times as long as wide; palp of Mx1 with broad shovel-shaped article 1; stout articles 3 and 2 of A2, article 3 about as long as wide and article 2 about 3 times as long as wide; P1 and P2 with short and wide merus, about 3 times as long as wide; PP5–7 with slender propodal segments, about 6, 7 and 10 times as long as wide, respectively; posterodorsal area of Pleonites 1 and 2 produced into 3 small teeth of which the median one is the longest; Urosomites 1 and 2 with wellmarked dorsal crest; Telson with long distal teeth, accompanied by 2 interdental long and slender spines.

Etymology

The species is named after its symbiotic lifestyle.

Type material

Holotype

PACIFIC OCEAN • ♀ (bl 6.5 mm); Sea of Japan, Primorye , Peter the Great Bay, Vostok Bay, in front of the scientific station “Vostok”; 42°54′35.8″ N, 132°44′08.7″ E; depth 1–1.5 m; 30–31 Jul. 2017; I. Marin leg.; shore in front of the laboratory, sandy-gravel bottom overgrown with sea grass; yabbypump; from burrows of spoon worm U. unicinctus ; ZMMU Mb-1153.

Paratypes

PACIFIC OCEAN • 1 ♂; same data as for holotype; ZMMU Mb-1154 • 1 ♀; same data as for holotype; GenBank: MN704855 , MN704856 ; ZMMU Mb-1155 .

Additional material

PACIFIC OCEAN • 8 ♀♀, 1 ♂; same data as for holotype; LEMMI • 5 ♀♀; Sea of Japan, Primorye , Posjeta Bay, Troitza Bay; 42°38′60.0″ N, 131°07′27.8″ E; depth 1–1.5 m; Jul. 2019; I. Marin leg.; muddy sand; inside burrow of spoon worm U. unicinctus ; yabby-pump; LEMMI • 1 ♀; Peter the Great Bay, Astafieva Bay; 42°36′52.2″ N, 131°12′01.1″ E; depth 1–1.5 m; Jul. 2019; I. Marin leg.; sand bottom; inside burrow of spoon worm U. unicinctus ; yabby-pump; LEMMI .

Description

HEAD ( Fig. 2c ). Rostrum turned downward, distally acute; eye large ( Fig. 1 ), with well-developed ommatidia, eye brightly white in alive specimens ( Fig. 1 ).

ANTENNA 1 ( Fig. 2d ). Article 3 stout, about 1.5 times as long as wide; article 2 about as long as wide, with dorsal projection produced into a rounded lobe; major flagellum with 15–17 articles; accessory flagellum with 10–11 articles.

ANTENNA 2 ( Fig. 2e ). Article 3 about as long as wide, unarmed; article 2 about 3 times as long as wide, with 4 small dorsal spines, with 1 long distodorsal and 2 long simple distoventral spines, with simple setae ventrally; article 1 about 4–4.5 times as long as wide, with small dorsal spines, with 1 distoventral long spine, unarmed ventrally; flagellum with 13–15 articles.

LABRUM ( Fig. 2a ). Upper lip with labrum broader than long and smaller than epistome, apical margin sinuous.

EPISTOME ( Fig. 2b ). With rounded lobes, protruding in lateral view, armed with small setae dorsally.

MANDIBLE ( Fig. 2f ). Lacinia mobilis large, anterior margin armed with 5 small strong teeth; palp consists of 3 long slender articles, similar in size, covered with long simple setae, article 1 almost equal to article 2, about 5–6 times as long as wide; article 2 about 5–6 times as long as wide; article 3 almost equal to articles 1 and 2, about 5 times as long as wide.

MAXILLA 1 ( Fig. 2g ). Outer plate with 8 large slender spines, ventrally denticulated; inner plate with a single long plumose seta; palp consists of 4 articles, article 1 shovel-shaped, with broad median part, about 1.5–2 times as long as wide, with 8–9 sharp robust spines along anterior margin, and simple small setae along dorsal margin.

MAXILLA 2 ( Fig. 2h ). Inner and outer plates distally rounded, robust, covered with numerous long simple setae along anterior and lateral margins.

MAXILLIPED ( Fig. 2i ). Palp consists of 4 articles: article 1 of palp unarmed, article 2 with a cluster of long setae distodorsally, small robust setae distally and long simple setae along the inner margin, outer margin unarmed; article 3 with a cluster of long simple setae along anterior border and distal part of inner margin, outer margin unarmed, article 4 (dactylus) slender, curved, about 0.8 times as long as article 3, unarmed; outer plate with 13–15 robust spines along medial border (distal spines are narrow and rather long); inner plate covered with small setae along anterior margin.

GNATHOPOD 1 ( Fig. 3a ). Coxa trapezoidal, with anterior medial setae only, posterior border weakly concave; basis slender, about 6–7 times as long as wide, with ventral projection in proximal part, with long simple setae; ischium about as long as wide, with long simple setae along distoventral border; merus about 1.5 times as long as wide, sharping distoventrally, with several groups of setae along ventral margin; carpus slender, with blunt distoventral process, reaching ⅓ of palm length, not reaching propodal group of strong spines, armed with several groups of setae; propodus about twice as long as wide both in male and females ( Fig. 3b ), with convex ventral margin, armed with small simple setae along almost all its length, with a depression and 3 long simple setae in proximal part level with end of dactylus, dorsal margin straight and unarmed; dactylus with 5–7 triangular teeth.

GNATHOPOD 2 ( Fig. 3c ). Very similar to Gn 1 in shape and slightly larger in size; coxa triangulo-elliptic; basis slender, about 6 times as long as wide, with long simple setae; ischium about as long as wide, with long simple setae along distoventral border; merus about 1.5 times as long as wide, sharpening distoventrally, with several groups of setae along ventral margin; carpus slender, with blunt distoventral process, reaching ¼ of palm length, not quite reaching propodal group of strong spines, armed with several groups of setae; propodus about 2 times as long as wide in both male ( Fig. 5a ) and females ( Fig. 3d ), dorsal margin straight and unarmed, with convex ventral margin, armed with small simple setae along almost entire length, with a depression and 3 long simple setae in proximal part level with end of dactylus; dactylus with 10–11 triangular teeth.

PEREIOPOD 3 ( Fig. 4a ). Coxa elliptic and narrow; basis slender, about 8–9 times as long as wide, with straight margins, covered with long simple setae; ischium about as long as wide, with long simple setae along distoventral border; merus broad, about 3 times as long as wide, slightly longer than carpus and equal to propodus, dorsal margin produced forward, with long simple setae along dorsal and ventral margins; carpus about 3 times as long as wide, with straight margins, unarmed dorsally and with simple long setae along ventral margin; propodus about 4–4.5 times as long as wide, slightly curved, unarmed dorsally and ventrally, with several long simple setae at distodorsal angle; dactylus of normal length, slender, weakly curved, slightly shorter than propodus and equal to carpus in length.

PEREIOPOD 4 ( Fig. 4b ). Coxa wide, with parallel anterior and posterior border, ventral border with 3 wellmarked serrations; basis slender, about 7–7.5 times as long as wide, with straight margins, covered with long simple setae; ischium about as long as wide, with long simple setae along distoventral border; merus broad, about 3 times as long as wide, longer than carpus and slightly shorter than propodus, dorsal margin produced forward, with long simple setae along dorsal and ventral margins; carpus about 2.5–3 times as long as wide, with straight margins, unarmed dorsally and with long simple setae along ventral margin; propodus about 5–5.5 times as long as wide, slightly curved, unarmed dorsally, with several long simple setae at distodorsal angle, with 5 tiny spines along ventral margin; dactylus of normal length, slender, weakly curved, slightly shorter than propodus and slightly longer than carpus.

PEREIOPOD 5 ( Fig. 4c ). Coxa subquadrate, with medially concave ventral margin, unarmed; basis broad, with anterior and posterior border convex; anterior border with 12–13 small spines accompanied by small setae, posterior border with well-marked serration; ischium about as long as wide, with large simple spine on anterodistal corner; merus about 4 times as long as wide, with 4 short anterior spines, 1 large distodorsal spine paired with a spinule, and 1 simple distoventral spine; carpus about 4 times as long as wide, slightly shorter than merus, unarmed posteriorly, with 3 small anterior spines, and with a distal pair of spines anteriorly and posteriorly; propodus ( Fig. 4d ) about 6 times as long as proximal width, slightly tapering distally, with 10 anterior spines and series of long medial setae; dactylus distinctly curved and of normal stoutness, with tip entire, about ½ of the length of propodus.

PEREIOPOD 6 ( Fig. 4e ). Coxa subquadrate, with medially concave ventral margin, unarmed; basis broad, with anterior and posterior border convex; anterior border with 10 small spines accompanied with small setae, posterior border with well-marked serration; ischium about as long as wide, with large simple spine on anterodistal corner; merus about 4 times as long as wide, with 5 short anterior spines, a pair of large distodorsal spines and 1 simple distoventral spine paired with a spinule; carpus about 4.5–5 times as long as wide, slightly shorter than merus, unarmed posteriorly, with 4 small anterior spines, and a distal pair of spines anteriorly and posteriorly; propodus ( Fig. 4f ) about 7 times as long as proximal width, tapering distally, with 4 long anterior spines and series of long medial setae; dactylus distinctly curved, sharp, about ⅓ of the length of propodus.

PEREIOPOD 7 ( Fig. 4g ). Coxa almost rectangular; basis greatly broad, almost round, with convex anterior border and strongly convex posterior border; anterior border with 12 small conical spines, posterior border serrated, distal border with strong long spine; ischium about as long as wide, unarmed; merus broad, about 2.5–3 times as long as wide, with 4 anterior small spines and pair of anterodistal simple spines, 3 posterior spines and a pair of long posterodistal long spines; carpus about 5.5 times as long as wide, slightly longer than merus, with single or paired anterior spines and long simple setae posteriorly; propodus about 10 times as long as wide, tapering distally, with 4 small anterior spines and long setae posteriorly; dactylus straight, very long and slender, entire, about ⅓ of the length of propodus.

PLEONITE 1 ( Fig. 5b ). Posterodorsal area produced into 3 small teeth of which median is longest ( Fig. 5e ); Ep1 with normally developed posteroventral tooth, with posterior border weakly convex, covered with numerous simple setae.

PLEONITE 2 ( Fig. 5b ). Posterodorsal area produced into 3 small teeth of which median is longest ( Fig. 5e ); Ep2 with normally developed posteroventral triangular tooth, with posterior border distinctly convex, covered with numerous simple setae.

PLEONITE 3 ( Fig. 5b ). Posterodorsal area toothless ( Fig. 5e ); Ep3 with small posteroventral tooth and distinct rounded notch ( Fig. 5c ), with posterior border convex.

UROSOMITE 1. With well-developed dorsal lamina and posterodorsal tooth ( Fig. 5d ); peduncle of U1 with medial distal corner rounded, with 4 dorsolateral spines of which proximal is longest, with 1 dorsomedial spine and 1 ventromedial spine; outer ramus with 5 small outer spines and 4 small medial spines; inner ramus with 4 small outer spines and 7 small medial spines.

UROSOMITE 2. With well-developed dorsal lamina and posterodorsal tooth ( Fig. 5d ); peduncle of U2 with 4 slender dorsolateral distal spines, with 1 dorsomedial spine and 1 ventromedial spine; outer ramus

with 5 small outer spines and 4 small medial spines; inner ramus with 4 small outer spines and 4 small medial spines.

UROSOMITE 3. With sharp medial projection ( Fig. 5i ), with 1–2 lateral spines, 1 long posterolateral tooth and 3 posterodorsal spines; outer ramus with 3–4 small outer spines and 4 small medial spines; inner ramus with 6 small outer spines and 4 small medial spines ( Fig. 5h ).

TELSON ( Fig. 2k ). With cleft reaching 0.85–0.9 of telson length; distal teeth about ¼ of the length of telson, medial teeth longer than outer teeth, 2 interdental spines long and slender, overreaching outer teeth.

COLORATION. General coloration of body and all appendages translucent white with large light and dark brown spots; some segments of appendages dark red or with dark red spots; eyes brightly white ( Fig. 1 ).

BODY SIZE. Largest collected female = bl 6.5 mm; largest collected male mostly similar in size to largest female, with bl 6.5 mm.

Taxonomic remarks

The new species is distinctly morphologically similar to L. geminata and L. serratoides . At the same time, the new species can be clearly distinguished by several morphological features not known from the latter species.

From L. geminata (see description, presented by Barnard (1969)), the new species can be distinguished by the following characters: smaller dorsal crest on urosomites 1 and 2 ( Fig. 5d ); Mx1 with wide, shovelshaped article 3 of palp ( Fig. 2h ); shorter and wider merus of P1 and P2 (see Fig. 4 a–b); slender propodal segments of PP5–7 (see Fig. 4 c–g); absence of long proximal seta of peduncle of U1 (see Fig. 5f ); shape of medial teeth of telson ( Fig. 2k ), which are significantly longer and accompanied by 2 long interdental spines. At the same time, L. geminata seems to be more closely related to the new species by its very similar body coloration, the presence of a small dorsal crest on urosomites 1 and 2, short articles of peduncle of A1, relatively stout distal segments of PP3–4 (especially merus), and other morphological features that clearly separate both species from their relative L. serratoides .

From L. serratiodes (after Tzvetkova 1967), the new species is easily separated by the following characters: presence of a dorsal crest on urosomites 1 and 2; stout articles of peduncle of A1 and A2 ( Fig. 2 d–e); wide distal article of palp of Mx1; stout and wider distal segments, especially merus, of PP1–2; slender propodal segment of PP5–7; length and shape of medial teeth of telson, which are significantly longer and accompanied by 2 long interdental spines. In addition, relatively stout and wide segments of PP3–4 are distinguishing features that separate the aforementioned species from tropical relatives, such as L. japonica and L. serrata (e.g., Nagata 1965; Azman & Othman 2013).

From L. japonica and L. serrata , known from the Seto Inland Sea in southern Japan (see Nagata 1965), the new species can be distinguished by longer rostrum, mandibular palp with longer and slender articles, especially distal one; shorter and stouter articles of peduncle A1 and A2; stouter distal segments of PP3–4, especially stout and wide merus of P3; significantly shorted dactyli of PP5–7; slender rami of U3 and longer median teeth of telson.

From Liljeborgia hwanghaensis Kim & Kim, 1990 , known from the Korean coasts of the Yellow Sea (37°23′ N, 126°35′ E) (see Kim & Kim 1990), the new species can be clearly separated by the posterodorsal armature of pleonites 1 and 2 (3 teeth in the new species vs 5 teeth in L. hwanghaensis ) and shorter median teeth of telson.

Habitat and ecology

Specimens of Liljeborgia associata sp. nov. were collected inside the burrows of Urechis unicinctus (Drasche, 1880) (Polychaeta: Echiura: Urechidae ), representing the first case of an association between liljeborgiid amphipods and spoon worms (Echiura).The spoon worm U. unicinctus lives in large U-shaped burrows constructed in muddy and sandy sediments in the inter- and subtidal zones in the Sea of Japan and the Yellow Sea ( Abe et al. 2014; pers. obs.). About 20% of the studied spoon worms burrows were inhabited by a single individual of the new species, which may indicate aggressive territorial behavior.

Distribution

The specimens of Liljeborgia associata sp. nov. were found in the southern part of the Peter the Great Bay and the northern part of Posjeta Bay in the Sea of Japan ( Russian Federation) (see Fig. 1 ), where the present study was accomplished. The distribution of the new species is probably related with the distribution range of its host, U. unicinctus (see Abe et al. 2014).

Key to the species of the family Liljeborgiidae from the boreal waters of the NW Pacific (with species of Liljeborgia from the NE Pacific)

1. Gn1 significantly larger than Gn2; U3 large, paddle-like; postero-dorsal margin of pleonites 2–3 armed with marked teeth; eyes absent. NW Pacific: Sakhalin, the Sea of Okhotsk, depth 109– 309 m ................................................................................................... Sextonia caecus Labay, 2017

– Gn1 similar to Gn2; U3 smaller than U1 and U2; postero-dorsal margin of pleonites 2–3 unarmed; eyes present (except L. cota ) ............................................................................................................ 2

2. Carpus of G1 and G2 with strongly produced slender ventral lobe extending along hind margin of propodus .......................................................................................3 ( Liljeborgia Spence Bate, 1862 )

– Carpus of G1 and G2 lacking produced ventral lobe. Known from the NE Pacific only ................... ................................................................ Idunella G.O. Sars, 1894 (= Listriella J.L. Barnard, 1959 )

3. Posterodorsal area of pleonites 1 and 2 produced into 5 teeth of which the median one is the longest. Known from the Korean coasts of the Yellow Sea .... Liljeborgia hwanghaensis Kim & Kim, 1990

– Posterodorsal area of pleonites 1 and 2 produced into 3 teeth of which the median one is the longest ............................................................................................................................................... 4

4. Telson cleft only ¼ to ⅓, lacking terminal spines on lobes of telson; basis of PP5–7 more than twice as long as wide; blind. NE Pacific: from the Gulf of Alaska to the northern Baja California, depth 366–2000 m ...................................................................................... Liljeborgia cota Barnard, 1962

– Telson cleft nearly to base, lobes with imbedded terminal spine; basis of PP5–7 about 1–1.5 times as long as wide; with eyes ................................................................................................................ 5

5. Epimeral plate 1 concave above postero-ventral tooth. From NE Atlantic to the coasts of Central California, depth 40–611 m ................................................................ Liljeborgia pallida Bate, 1857

– Epimeral plate 1 convex above postero-ventral tooth ...................................................................... 6

6. Cusps of lobes of the telson longer medially than laterally; eyes reniform. NE Pacific: from Bahia de Los Angeles, Gulf of California, depth 46 m ....................... Liljeborgia marcinabrio Barnard, 1979

– Cusps of lobes of the telson subequal longer laterally than medially; eyes oval to subquadrate ..... 7

7. Urosomites 1–2 with well-marked dorsal crest, peduncle of A1 with short and stout articles (article 3 about 1.5 times as long as wide; article 2 about as long as wide) ................................................. 8

– Urosomites 1–2 without dorsal crest, peduncle of A1 with slender articles (article 3 about 2–2.5 times as long as wide; article 2 about 1.5 times as long as wide). NW Pacific: Posjeta Bay in the Sea of Japan, intertidal ............................................................. Liljeborgia serratoides Tzvetkova, 1967

8. Medial teeth of telson about 0.15 length of telson, less than 1.5 times longer than outer teeth and accompanied by 1 long interdental spine. NE Pacific: from Goleta to the northern Baja California, depth 3–70 m ............................................................................ Liljeborgia geminata Barnard, 1969

– Medial teeth of telson about 0.25 length of telson, about 2 times longer than outer teeth and accompanied by 2 long interdental spines. NW Pacific: the Peter the Great Bay and the northern part of Posjeta Bay in the Sea of Japan, intertidal ...................................... Liljeborgia associata sp. nov.

Some other species of the genus Liljeborgia are known from the region and the Sea of Japan (e.g., Ishimaru 1994; Ren 2007). For example, Ishimaru (1994) notes Liljeborgia aequabilis Stebbing, 1888 from the tropical part of the Seto Inland Sea influenced by the Kuroshio Current. This species is actually recognized in Australia, New Zealand and the Sulu Sea as a common associate of hermit crabs ( Stebbing 1888; after Hurley 1954; see also Vader 1995) and by most morphological features, especially long and slender segments of PP3–4 and the form of telson (see above), belong to the tropical representatives of the genus, such as L. japonica and L. serrata , or possibly represent an undescribed species. These species are known from warm (tropical) waters and probably are not present in the boreal zone of the northern Pacific Ocean.

Figures

Fig. 1. Habitus of live female specimen of Liljeborgia associata sp. nov. from Vostok Bay of the Sea of Japan with geographical indication of the collection sites in the Peter the Great Bay and Posjeta Bay of the Sea of Japan.

Fig. 2. Liljeborgia associata sp. nov., female (LEMMI) from Vostok Bay of the Sea of Japan. a. Upper lip. b. Lower lip. c. Head. d. Antenna 1. e. Antenna 2. f. Mandible. g. Maxilla 1. h. Maxilla 2. i. Maxilliped. j. Pleopod 1. k. Telson.

Fig. 3. Liljeborgia associata sp. nov., female (LEMMI) from Vostok Bay of the Sea of Japan. a. Gnathopod 1. b. Chela of Gn1. c. Gnathopod 2. d. Chela of Gn2.

Fig. 4. Liljeborgia associata sp. nov., female (LEMMI) from Vostok Bay of the Sea of Japan. a. Pereopod 3. b. Pereopod 4. c. Pereopod 5. d. Distal segments of P5. e. Pereopod 6. f. Distal segments of P6. g. Pereopod 7.

Fig. 5. Liljeborgia associata sp. nov., male (a) (LEMMI) and female (b–i) (LEMMI) from Vostok Bay of the Sea of Japan. a. Chela of Gn2. b. Pleonites 1–3 and urosomites 1–3. c. Ventroproximal margin of pleonite 3. d. Urosomites 1–3 and telson. e. Dorsoproximal margins of pleonites 1–3. f. Uropod 1. g. Uropod 2. h. Uropod 3. i. Peduncle of uropod 1, outer view.