Chone infundibuliformis Krøyer, 1856

Figures 1–3, 4 A –C, 5–11

Chone infundibuliformis Krøyer, 1856, 33.— Malmgren, 1866: 404 —405, Pl. 28, Fig. 87.— Malmgren, 1867: 116.— Cunningham and Ramage, 1887: 670, Pl. 44, Fig. 32.— McIntosh, 1916: 35, Pl. 2, Fig. 9.— Fauvel, 1927: 334, Fig. 116 a –o.— Wesenberg­Lund, 1950, 58.— Banse, 1972: 461 –465, Fig. 1 a –l.— Hartmann­Schröder, 1996: 550, Fig. 168 a –h.

Type material: Lectotype [ ZMUC POL – 1749] Greenland, locality unknown, Leg. Krøyer. Paralectotypes [ USNM 376] Greenland, locality unknown, Leg. Krøyer, not Lutken ( 2). Paralectotypes [ BMNH 82.5.12.33] Greenland, locality unknown, Leg. Krøyer, not Lutken ( 3).

Non­type material: Greenland [ BMNH] 1921.5.1.4364, 4368 / 69 Greenland, Godhaven Harbour, “Valorous”, 9–18 m ( 5). 1921.5.1.4364, 4368 / 69 Greenland, Bressay Sound, Coll. Mc Intosh, 1921, 5, 1–436 K ( 2). No number, Press. J. Berryman, Coll. Yell, Shetland, Whaal Firth in silt, 1979 / 80 ( 3). [ LACM – AHF] 0 0 3224 Goodhvan Fjord, dredged, Kristineberg Zool. Station ( 4). [ MCZ] North Atlantic Ocean, R/V Albatross IV, Cruise 9809, Sta. 187, July 29, 1998, NMFS 1999 ( 1). [ SMNH] 6861, 73073 W Greenland, Egedesminde, Leg. O. Torell ( 1). 6862, 73074 W Greenland, Godhavn, 55 m, 69 ° 14 ’ N, Leg. C. T. Amondsen ( 2). [ ZMB] 3106 Grönland, Karajak, Fjord. Leg. Vanhöffem S, July, 1893 ( 4); July 21, 1893 ( 1). 5167 Grönland, Coll. Grube/Oersted S. ( 3). 5168 Spitzbergen, Coll. Grube/Malmgren S. ( 1). [ ZMUC] POL – 1761 Lille Hellefiskebanke, 4 miles W. S. W. of Rifkol, July 10, 1912, 40 m, Coll. Bornemann ( 1). POL – 1764 East of Greenland, 4 th Thule Expedition Sta. 26, Kangerolussuaq, August 20, 1933, 1–5 m ( 2). POL – 1765 East of Greenland, 4 th Thule Expedition Sta. 29, Kangerolussuaq, August 25, 1933, 4–5 m ( 28). Norway [ SMNH] 6864, 73076 Svalbard, Vest Spitzbergen, Hornsund, 73 m, Leg. Swedish Arctic Expedition, 1864 ( 2). [ ZMB] 1986 Spitzbergen, Kükenthal S. G. ( 2). [ ZMB] 6226 Spitzbergen, Exp. Rómer & Schaudinn S. Sta. 12 ( 1); Sta. 13 ( 3); Sta 14 ( 1); Sta. 36 ( 3); Sta. 41 ( 2); Sta 513 ( 2). Canada [ CMN] 3867 Byam Martin Channel, Sta. 10, 75 ° 01.4’ N, 106 ° 35 ’ W, R. K. S. Lee, July 14, 1974 ( 2). 3870 Byam Martin Channel, 74 ° 58.8’ N, 106 ° 23.5’ W, Sta. 2, Coll. R. K. S. Lee, June 18, 1974 ( 1). 1980 –0171 New Foundland, Labrador Nain, 56 ° 36 ’ N, 62 ° N, Sta. SAR 3–528 B, Coll. J. Barrie, September 11, 1977 ( 1). 1982 –0938 North West Territories, Davis Strait, 61 ° 10 ’ N, 61 ° W, Coll. Mac Laren Atlantic, October 23, 1976, Sta. 25 ( 3). 1988 –0364 New Foundland, Labrador Shelf, Sta. 4, 53 ° 19 ’ N, 54 ° 41 ’ W, 350 m, Coll. D. Peer, Habitat Ecol Lab, September 5–6, 1987 ( 1). 1993 –0030 Sta. B – 2, Coll. Arctic Biol. Sta. Ste. Anne de Bellevue, 1949 –00–00 ( 1). 1993 ­0031 Sta. 67 – 5. Coll. Arctic Biol. Sta. Ste. Anne de Bellevue, 1967 –00–00 ( 3). 1993 –0032 Frobisher Bay, Baffin, Sta. 5 b, 63 ° 43.5’ N, 68 ° 31.7’ W, 13–23 m, Coll. Arctic Biol. Sta. Ste. Anne de Bellevue ( 2). 1995 –0570 Sta. Theron, Th – 451 – 45, Coll. Arctic Biol. Sta. Ste. Anne de Bellevue, September 0 1, 1965 ( 3). 1995 –0571 Sta. Theron, Th – 490 VVG – 49, Coll. Arctic Biol. Sta. Ste. Anne de Bellevue, September 8, 1965 ( 5). NFLD Sta. 517, 51 ° 22 ’ N, 50 ° 21 ’ 31 ’’ W. Coll. S. W. Gorham, May 28, 1963, 360 m, Set. 134 ( 2). “Calanus” 1949 B – 11 ( 1).

Additional material: Chone americana Day, 1973 [ FSBC EJ 71414] Eastern Florida, St. Lucie County, Hutchinson Island, East of F. P. and L. Electrical generating plant, 27 ° 21 ’ 23 ’’ N, 80 ° 13 ’ 24 ’’ W, 11.2 m. Chone aurantiaca ( Johnson, 1901), holotype [ MCZ 1933] Port Orchard, Puget Sound, Washington, Coll. A. Robertson, July 4, 1898. [ LACM – AHF] West Seattle, Washington, Vashon Island, Ferry dock, May 7, 2004, intertidal, Coll. B. Pernet. Chone farringtonae Tovar­Hernández, 2005, paratype [ FSBC I 66734] West Coast of Florida, off shore Pinellas County, Boca Ciega Bay, June 17, 1976. Chone georgesi Fitzhugh in press [ECOSUR] Isla Mujeres, Bajo Pepito, Mexico, in Stypopodium zonata, Coll. M. Díaz, February 1997. Chone gracilis Moore, 1906, holotype [ USNM 5513] Alitak Bay, Kodiak Island, Alaska, Sta. 4274 ( 1903), 7.2– 42 m. Chone magna ( Moore, 1923), holotype [ USNM 17281] Off Harris, Pt. San Miguel, California, Albatross R/V, Sta. 4436, April 15, 1904. Chone mollis ( Bush, 1904), holotype [ YPM 2793] Harriman Alaska Expedition, Pacific Grove, California, Coll. W. R. Coe, 1901. Chone picta Verrill, 1885, topotype [ YPM 30002] Martha’s Vineyard, Massachusetts. 70 ° 51 ’ N, 41 ° 22 ’ W. Coll. J. L. Simon and P. E. Schwamb, June 22, 1966. Chone princei McIntosh, 1916, topotype [ CMN 1989 –0394] Quebec, St. Lawrence estuary, off Point Mitis, 37 m, Sta. B 610 – 7 IL – 152 D, Coll. Rafat MASSAD, July 0 9, 1971.

Redescription

The following redescription is based mainly upon the lectotype. Numbers in parentheses correspond to variation among paralectotypes and additional material.

Colour, body shape and size: Body cream colored (specimen from North Atlantic Ocean pink when collected, MCZ, R/V Albatross IV), trunk cylindrical ( Fig. 1). Body length: 81 mm ( 12–103), width: 8 mm ( 1–10). Tubes composed of fine sand.

Branchial lobes and branchial crown: Branchial lobes medium­sized, located in lateral position on either side of mouth, curved such that they are concave in cross section relative to the mouth, insertion not exposed beyond collar ( Figs 1 A –B). Branchial crown length: 19 mm ( 11–90). Radioles: 24 ( 7–23) pairs. Each radiole with paired series of pinnules of different size; median pinnules 3 times longer than more proximal pinnules. Radiolar tips: short­sized ( Fig. 2 B). The palmate membrane extends up three quarters of the branchial crown length. Lateral flanges broad ( Figs 2 A –B), outer radiole surfaces flat ( Fig. 2 A). Dorsal lips extend from the inner, dorsal margins of the branchial lobes and terminate just dorsal to mouth ( Fig. 5 A), broadly rounded in frontal view, as long as wide, without mid­rib, resembling the ventral lips ( Fig. 1 I), longer than wide in dorso­lateral view ( Figs 1 E –F, H); dorsal lips vascularized by a plexus of small blood vessels derived from basal branchial blood vessels ( Fig. 6 A –B); filled with hyaline cartilage ( Figs 7 A –C, E), no extension of branchial skeleton. Dorsal margin of dorsal lips extends up along inner margin of dorsalmost radiole, fused with 8 ( 5–9 – 10) dorsal pinnular appendages united by a palmate membrane ( Fig. 1 E). Ventral lips rounded, as long as wide, about half of the dorsal lips length, extending from the central margin of the branchial lobes ( Fig. 1 H), filled with hyaline cartilage ( Figs 8 A –C). Ventral radiolar appendages: 6 ( 3–7) pairs of similar length, about one quarter of the branchial crown length, originate just ventral to ventral lips ( Figs 9 A –B), continuous with ventral extensions of inner margins of branchial lobes ( Fig. 1 H).

Peristomium: Anterior peristomial ring lobe not exposed beyond collar, distally entire, triangular. Posterior peristomial ring collar: antero­dorsal, lateral and ventral margins entire, ventral margin slightly higher than dorsal ( Figs 1 A –B), entire length of mid­dorsal collar margins form a narrow gap. Ventral shield of collar swollen, horseshoe­shaped, two times wider than long; ventral shield divided transversally by a white and slender line, the anterior half transparent ( Fig. 1 A). The posterior peristomial ring collar length is as long as 1.5 times the length of chaetiger 2 in lateral view.

Thorax: Chaetiger 1: Notopodia: two groups of 14–16 chaetae, chaetae from the exterior group twice longer than interior group ( Fig. 3 A). Chaetigers 2 to 8: Notopodia: superior group with two irregular rows of elongate, narrowly hooded chaetae, each row with 30 ( 26–42) chaetae ( Fig. 3 B); inferior group with one anterior row with 16 ( 18–28) short bayonet chaetae ( Figs 3 B –C), 2 posterior rows with 22 ( 31–43) symmetrical, paleate chaetae with short mucro ( Figs 3 B –C). Pre­ and post­chaetal lobes well developed ( Fig. 3 B). Neuropodia: 29 ( 39–45) acicular uncini per tori, distributed as an irregular double row (except in juveniles); heads in the same direction ( Fig. 3 F); the oldest upper parts of the tori have only one row (one quarter of the tori length); main fang surmounted by four rows of teeth in frontal view, occupying less than half of the main fang length; teeth unequal in size ( Fig. 4 A). Biannulate condition in thoracic segments is given by the presence of well differentiate intersegmental grooves, and inter­notopodial and interneuropodial grooves, less differentiated than intersegmental ( Figs 1 A –B). Glandular ridge on chaetiger 2, narrow, just below chaetal lobe and tori ( Figs 1 A –B, 2 C, 11 A, F –G).

Abdomen: Abdominal segments: 44 ( 28–76). Anterior segments: two transverse rows of 22 elongate, narrowly hooded chaetae, chaetae from the upper row half as long as chaetae in lower row ( Figs 3 D –E); 25 ( 29–33) uncini per tori ( Fig. 3 G), older and younger uncini with the main fang surmounted by five rows of teeth in frontal view, occupying less than half of the main fang length ( Fig. 4 B), main fang not extending beyond breast ( Fig. 1 G). Posterior segments: 23–28 very elongate, narrowly hooded chaetae, 25 % longer than those of anterior segments ( Fig. 3 E); 3 ( 3–4) uncini per torus, similar to anterior segments, but shorter ( Figs 1 J, 4 C). Intersegmental grooves well differentiate, inter­notopodial and inter­neuropodial grooves less differentiated than intersegmental. Pygidium with rounded posterior margin ( Fig. 1 D).

Gametes: Lectotype is a female, oocytes in all thoracic and abdominal segments, diameter 6.07 m. Specimens from CMN 3870 are females with oocytes distributed in all thoracic and abdominal segments; males with sperm in anterior abdominal chaetigers, spermatids develop in tetrads, and mushroom­shaped acrosom.

Methyl green staining: The epidermis is completely glandularized and stains uniformly in thorax and abdomen, dorsal and ventrally, except in except intersegmental grooves, inter­notochaetal and neurochaetal grooves, and both pre and post­chaetal lobes ( Figs 1 A –B). The collar segment is darker in the anterior half, except for anterior end of the ventral shield of collar.

Remarks: Scanning electron microscopy revealed an important character in this species: teeth above the main fang of thoracic acicular uncini are of unequal size ( Fig. 4 A). Fitzhugh ( 1989) thought that all the teeth above main fang were of the same size, and that the presence of unequal­sized teeth was a synapomorphy for Amphicorina Claparède, 1864. This character is, however, homoplastic, occurring in most of the fabriciin genera, and its presence is now documented in C. infundibuliformis, C. georgesi ( Fig. 4 D), C. americana ( Fig. 4 G) and C. farringtonae ( Fig. 4 J). In C. infundibuliformis, the only feature that tends to be dependent on size and age is the presence of thoracic uncini distributed as irregular double row in adults ( Fig. 3 F), while in juveniles there is only one row of uncini per torus.

The presence of modified uncini in posterior abdominal segments as rasp­shaped plates or Amphicorina ­ type (see Rouse 1994: Fig. 17) have been recorded or illustrated in some species of Chone: C. longiseta Giangrande, 1992, C. acustica Claparède, 1870, and C. filicaudata Southern, 1914 (in Giangrande 1992); C. trilobata Gallardo, 1968, C. sp. 1, C. sp. 2, C. sp. 3, C. sp. 4 and C. sp. 6 (in Fitzhugh, 2002); C. americana Day, 1973, C. diazi, C. farringtonae, C. johnstonae, C. perkinsi and C. uebelackerae ( Tovar­Hernández, 2005). This kind of modified uncini ( Figs 4 F, I, L, O) have a main fang surmounted by several regular, vertical rows of small teeth of equal size that occupy at least three quarters of the main fang length, and a poorly developed rectangular or sub­rectangular breast, instead of a few rows of unequal­sized teeth occupying less than half of the main fang length and a well developed breast, as anterior segment uncini ( Fig 4 E, H, K, N). However, anterior and posterior abdominal uncini are similar in shape in the type species. They possess a well developed main fang surmounted by a few smaller teeth that occupy less than half of its length ( Figs 4 B –C) and are irregularly arranged in an overlapping pattern, instead of a uniform set of rows ( Fig. 4 C). The breast is well developed and main fang does not extend beyond it. Other species reviewed with anterior and posterior abdominal uncini of similar shape include: C. aurantiaca [ MCZ 1933, holotype], C. gracilis [ USNM 5513, holotype], C. magna [ USNM 17281, holotype], C. mollis [ YPM 2793, holotype] and C. picta [ YPM 30002].

In those species of Chone with modified, posterior abdominal uncini, the presence of a posterior, latero­ventral depression is easily seen (see Tovar­Hernández 2005, Fig. 11 B); however, this depression is not the same as the anal depression in Euchone Malmgren, 1866. In Euchone, the anal depression (=anal plate, funnel, spoon­shaped cavity or scoop) is ventral and extends from the pygidium through a varying number of abdominal chaetigers ( Fitzhugh 1989). Cochrane ( 2003) recognized the anal depression as either being bordered by lateral wings or clearly demarcated by anterior and/or lateral ridges; she also detected a degree of ambiguity between a posteriorly enlarged faecal groove or dorsoventral depression in certain Chone and Amphicorina species, and a poorly developed anal depression in some Euchone. In species of Euchone, the Amphicorina ­ type abdominal uncini are primarily located in the area of the anal depression ( Banse 1970; Fitzhugh 1989); in species of Chone with modified abdominal uncini ( C. georgesi ( Fig. 4 F), C. americana ( Fig. 4 I), C. farringtonae ( Fig. 4 L) and C. princei ( Fig. 4 O)), they are also located in the segments of the latero­ventral depression.

Histology

Gross observations

The branchial crown in C. infundibuliformis is supported basally by a central mass of cartilaginous skeleton and two lateral bars or horns of cartilaginous skeleton, both completely separated, independent one of another. i) The basal central mass of cartilaginous skeleton ( bcs) is located above the sub­esophageal ganglia ( Figs 5 A, 6 A), divided basally and covered antero­laterally by smooth muscle ( m) ( Fig. 6 A). ii) The lateral bars or horns of cartilaginous skeleton ( bls) are composed of a large mass of cells in the base of the branchial lobes extending through radioles as two rows of cells ( Figs 5 A, 6 A).

The branchial crown is vascularized by two large blood vessels ( bv) ( Figs 5 A, 6 A); each vessel is covered by a coelomic chamber ( cc) and conjunctive tissue ( ct) ( Fig. 5 C). The branchial crown is innervated ( n) at the base of each branchial lobe ( Figs 5 A, D, 6 A) and supported with hyaline cartilage on lateral sides of mouth ( m) ( Fig. 5 A). The hyaline cartilage is constituted of chondrocytes ( c) and a homogeneous eosinophilic matrix ( cm) ( Fig. 5 E). Some muscular fibers ( mf) are disposed in dense bundles in different directions ( Fig. 5 B).

Dorsal lips and dorsal pinnular appendages

The dorsal lips are vascularized by a plexus of small blood vessels ( bv) than run along the lip as strongly branched network ( Figs 6 B –C, 7 A); each blood vessel is surrounded by coelomic chambers ( cc) ( Figs 6 B –C). These blood vessels are derived from the basal branchial blood vessels, which further back communicate with the dorsal vessel ( Fig. 6 A). The dorsal lips have hyaline cartilage, but there is no extension of the branchial skeleton. The hyaline cartilage ( hc) extends into the middle region of the dorsal lip and along the inner lip margin ( Fig. 7 A); it is composed of abundant collagen fibers ( cf) forming a net, and spread condrocytes ( c) ( Figs 7 A –C, E). The dorsal lips have conjuntive tissue ( ct) extending along the outer margin of the lip ( Figs 6 B –C, 7 A). Two types of simple epithelium are present in dorsal lips: columnar ( gce) and cubic ( gcue) ( Fig. 7 B). The columnar epithelium covers the external/outer margin of the lips ( Figs 6 B –C, 7 B), includes ciliated cells ( ci) ( Figs 6 B –C) and type “c” glands ( Fig. 7 B), and is covered by cuticle ( cu) ( Figs. 6 B –C, 7 B). The cubic epithelium covers the internal/inner margin of the lip ( Fig. 7 B), there are not ciliated cells ( Fig. 6 B –C), but contains types “a” and “b” glands, and is covered by cuticle ( Figs 7 B, D).

The external pinnula of each dorsalmost radiole is fused with six pinnules ( dpa) towards the dorsal, central margin of the branchial crown, above of the basal, central skeleton ( Figs 5 A, 6 A); they are united by a glandular, columnar epithelium composed of ciliated and types “b”, “c”, “d” glands. Each dorsal pinnular appendage contains a central blood vessel surrounded by the coelom, and associated with the pinnular skeleton and hyaline cartilage ( Fig. 7 F).

Ventral lips and ventral radiolar appendages

The ventral margins of the ventral lips are each fused with three undeveloped radioles ( unr) ( Fig. 8 A –B). The ventral lips are composed of hyaline cartilage ( hc) ( Figs 8 A –C) and ciliated epithelium and type “c” glands.

Radioles

The epithelium of radioles is simple columnar, covered by cuticle ( cu) and composed of type “c” glands ( Figs 9 A –B). One pair of nerves ( n) is between each pair of radioles ( Fig. 9 A). In cross section, the radiolar skeleton ( rs) is covered by hyaline cartilage, composed of a dense cartilage matrix ( cm) with few chondrocytes ( c) ( Fig. 9 C); in transversal section, the radiolar skeleton ( rs) continues into each pinnule ( ps), which is divided by longitudinal muscle ( m) and conjunctive tissue ( ct) ( Fig. 9 D). Directly from the branchial blood vessel, which further back communicates with the dorsal vessel, a small blood vessel branches off to each radiole and then, into each pinnule, surrounded by a coelomic chamber ( cc) ( Fig. 9 E). In cross section, each radiole is composed of a central endoskeleton axis consisting of two large cartilaginous cells ( rs) ( Fig. 9 A), longitudinal muscle ( m) and two pairs of nerves ( n) running along the basal groove, and ciliated epithelium in the basal groove of the radiole ( ci) ( Figs 9 A, D –E).

Collar

The mid­ventral margin of the posterior peristomial ring collar consist of a broad central axis of hyaline cartilage ( hc), including the area of the ventral shield of collar ( vsc) ( Fig. 10 A); composed of a dense cartilage matrix ( cm) with few chondrocytes ( Figs 10 A, D –E) and covered on both sides by glandular epithelium with types “a”, “b” and “c” glands (markedly basophilic and substantially larger) and cuticle ( cu) ( Figs 10 A –C).

Epithelium and glandular ridge on chaetiger 2

The epithelium of Chone infundibuliformis has type “a”, “b” and “c” glands markedly basophilic and substantially larger, covered by cuticle ( cu) ( Figs 11 A, D –F). Each intersegmental division is reinforced with conjunctive tissue ( ct) and nerves ( n) ( Fig. 11 B). At the base of the epithelium, there are several nerves ( n) and blood vessels ( bv) ( Figs 11 A, C). The glandular ridge in C. infundibuliformis and C. aurantiaca occupies only the external half of the epithelium; it is composed of strongly differentiated acidophil glandular cells ( ag), tubular­shaped with granulose secretions ( Fig. 11 A, G, 12 A –D).