Phoronopsis californica Hilton, 1930

Hirose, Masato & Uyeno, Daisuke, 2024, First record of Phoronopsis (Phoronida) from Japan, with a description of Phoronopsis californica Hilton, 1930 from Okinawa, Biodiversity Data Journal 12, pp. e 131280-e 131280 : e131280-

Phoronopsis californica Hilton, 1930

Phoronopsis californica Hilton, 1930 - Hilton (1930), 154–158; Emig (1969), 479–482, Figs. 10–13; Emig (1971), 554–555, Pl. 3, Figs. 8–9, Pl. 6, Figs. 5–8, Pl. 7, Fig. 11; Emig (1973), 17–20, Figs. 8 g – m, 9, 10; Temereva et al. (2016), 521, Fig. 32.

Materials

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1028 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: preserved in 70 % ethanol; disposition: in collection; occurrenceID: 54CFF287-778C-5937-AE70-1837CA5DDC26; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Oura Bay, Okinawa, Japan ; verbatimDepth: 6 m; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 27-07-2013; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: single upper part of individual including lophophore

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1029 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: fixed with 10 % formalin and preserved in 70 % ethanol; disposition: in collection; occurrenceID: 3DF81EA3-A31B-53C8-A1CA-8038C8B04CFB; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: individual

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1030 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: fixed with 10 % formalin and preserved in 70 % ethanol; disposition: in collection; occurrenceID: 49663507-1E6B-5DFC-AA2C-8125A022A320; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: individuals

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1031 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: fixed and preserved in 10 % formalin; disposition: in collection; occurrenceID: 94EE2857-5F54-5237-947E-30EFB70DDEA1; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: dissected individual

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1032 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: fixed and preserved in 10 % formalin; disposition: in collection; occurrenceID: 13C7149E-F548-5FD0-B58A-1BAF572C526F; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: dissected individual

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1033 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; preparations: fixed and preserved in 99 % ethanol; disposition: in collection; occurrenceID: 006A899A-3AA4-5917-AD27-364A5FC6ADDC; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: empty tube

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1034 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; preparations: fixed and preserved in 99 % ethanol; disposition: in collection; occurrenceID: 25D80D46-5EB8-5B3F-8A67-81D8D84D8BCA; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: empty tube

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1035 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; preparations: fixed and preserved in 99 % ethanol; disposition: in collection; occurrenceID: 2F908976-6845-5C0D-809A-31957348DDE7; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: empty tube

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1036 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; preparations: fixed and preserved in 99 % ethanol; disposition: in collection; occurrenceID: AD4B02A4-4761-5198-8FE7-EE51981D6580; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen; informationWithheld: empty tube

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1037 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: 20 slides of 6 - μm transverse sections stained with HE; disposition: in collection; occurrenceID: 83B05256-0FC6-536E-B8A0-D1E5E2F84A2C; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1038 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: 8 slides of 6 - μm transverse sections stained with HE; disposition: in collection; occurrenceID: F07C5C9E-22DF-543B-9AD3-75A21EB0B9AC; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1039 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: 16 slides of 6 - μm longitudinal sections stained with HE; disposition: in collection; occurrenceID: A7819A85-F858-53DB-BEA6-4D6DEB53DC72; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen

Type status: Other material. Occurrence: catalogNumber: NSMT-Te 1040 ; recordedBy: Masato Hirose, Daisuke Uyeno; individualCount: 1; lifeStage: adult; preparations: 20 slides of 6 - μm longitudinal sections stained with HE; disposition: in collection; occurrenceID: DDA70FBC-2DBF-5280-BE54-A66B3D194BAA; Taxon: scientificName: Phoronopsis californica Hilton, 1930 ; kingdom: Animalia; phylum: Phoronida; genus: Phoronopsis ; specificEpithet: californica ; scientificNameAuthorship: Hilton, 1930; nomenclaturalCode: ICZN; Location: country: Japan; stateProvince: Okinawa; locality: Kyoda, Nago Bay, Okinawa, Japan ; verbatimDepth: 5–10 m; verbatimCoordinates: 26°32'50.61"N, 127°57'41.06"E; Identification: identifiedBy: Masato Hirose; Event: samplingProtocol: SCUBA; eventDate: 22-02-2014; Record Level: language: en; ownerInstitutionCode: NSMT; basisOfRecord: PreservedSpecimen

Description

Body, except lophophore 27.62–116.56 mm in length (avg. 73.85 ± 31.52 mm, n = 5) in contracted state; 2.79–4.58 mm in diameter at ampula (avg. 3.77 ± 0.91 mm, n = 3); other parts ranged 1.25–3.90 mm in diameter; orange or brown with white spots in living state (Figs 2 , 3 ), yellowish-white after fixation (Fig. 4 A). Lophophore spirally-shaped in juvenile and helicoidal-shaped in adult with 6–10 coils on each side (Fig. 4 ); 5.13–15.41 mm in length (avg. 9.48 ± 4.04 mm, n = 7), 1.82–3.40 mm in diameter basally (avg. 2.60 ± 0.61 mm, n = 7); tentacles more than 1600 in number; orange or brown with white spots in life. Inhabits a cylindrical tube constructed with small sand grains (Fig. 4 B); 75.43–209.70 mm in length (avg. 119.52 ± 52.77 mm, n = 5); 7.00– 15.41 mm in diameter (avg. 7.88 ± 0.56 mm, n = 5). Single individual observed bearing an additional arm of lophophore was considered a morphological malformation (Fig. 5 ). Anal papilla densely covered with white pigments (Fig. 3 B).

Nephridia 762–888 μm in height (avg. 825 ± 89 μm, n = 2), with long slightly curved ascending branch (ab) and short descending branch (db) (Fig. 6 ), ab / db length ratio 2.6 (n = 2). Nephridial pore situated same or slightly above the anus level on the invagination of collar fold (Fig. 6 ), opening against intestine, about 24 μm in diameter (Fig. 7 C). Ascending branch located near intestine, lying on the body axis, slightly curved along the body wall (Fig. 6); 648–888 μm in height (avg. 768 ± 170 μm, n = 2). Descending branch situated the lower part of the nephridium, on the oesophagus side of ascending branch; 234–462 μm in height (avg. 348 ± 161 μm, n = 2). Two nephridial funnels present; anal funnel slightly larger than oral funnel in height; 126–156 μm (avg. 141 ± 21 μm, n = 2) and 102–162 μm (avg. 132 ± 42 μm, n = 2), respectively. The aperture of nephridial funnels located on lateral surface of upper part of descending branch; the anal funnel faces intestine, while the oral funnel faces oesophagus (Figs 6 , 7 D – F). Oral funnel situated slightly lower than anal funnel.

Body-wall longitudinal muscles of feathery type (Fig. 7 A and 7 B); 226–262 in number, arranged as in the following formula ( Selys-Longchamps 1907):

Composite formula Mean formula

[226–262] 243.5 = (n = 4 sections from 2 individuals)

Left and right lateral mesenteries present (Fig. 7 A). Single left giant nerve fibre present; transversally oblong, 62.0–72.0 μm wide and 92.9–123.5 μm long (avg. 670 ± 7.1 μm and 108.2 ± 21.6 μm, respectively, based on two sections from different parts of the body, from single individual), situated at the base of left lateral mesentery below the nephridial level (Fig. 7 B).

Gonads not observed in any of our specimens; sex could, thus, not be determined.

Distribution

Phoronopsis californica was originally described from the Balboa Bay, Los Angeles in USA and distributed along the west coasts of North America, coast of Spain, Madagascar, Mozambique Channel and the South China Sea ( Emig 1969, Emig and Plante 1969, Emig 1971, Emig 1973, Thomassin and Emig 1983, Sánchez Tocino et al. 1997, Temereva 2009, Temereva et al. 2016). From Japan, this species is known only from a soft sandy-mud bottom in the inner area of Oura Bay and Nago Bay, Okinawa.

Taxon discussion

Our material of Phoronopsis californica collected from Okinawa agrees with previous morphological accounts of this species ( Hilton 1930, Emig 1969, Emig 1971, Emig 1973) in the following characters: 1) the large helicoidal-shaped lophophore with bright colours in adult individuals, 2) nephridium with the long ascending branch and two nephridial funnels on the descending branch and 3) the number of longitudinal muscles in the left anal and both oral coeloms. All of our specimens have a remarkably shorter body length compared to that of P. californica (220–450 mm) previously reported ( Emig 1979), which is probably due to the contracted state and / or incomplete specimens. Some of our specimens are spirally-shaped; those specimens were probably a juvenile. Our specimens have a slightly larger number of longitudinal muscles in the right anal coeloms compared to the previous descriptions and the difference of height of oral and anal nephridial funnels are relatively smaller. Temereva et al. (2016) reported P. californica from the South China Sea; however, the identification is only based on the underwater photograph. This is the first record of the internal morphology and molecular data of P. californica from the north-western Pacific.

Figures

Figure 2. Phoronopsis californica Hilton, 1930. A Living adult individual found in Nago Bay (NSMT-Te 1029); B living juvenile individual with dark colour lophophore found in Nago Bay (NSMT-Te 1031).

Figure 3. Phoronopsis californica Hilton, 1930. A Oral view of anterior part of the body of living adult individual (NSMT-Te 1029); B anal view of anterior part of two juvenile individuals of different colour; both showing white pigmented anal papilla (NSMT-Te 1032, 1031). Scale bars: A = 1 cm; B = 5 mm.

Figure 4. Phoronopsis californica Hilton, 1930. A Preserved individual (10 % formalin seawater); B living individual in a dissected tube. Scale bars: 1 cm.

Figure 5. Phoronopsis californica Hilton, 1930, NSMT-Te 1030, bearing additional arm of lophophore (black arrowhead).

Figure 6. Reconstructed three-dimensional images of the nephridia of Phoronopsis californica Hilton, 1930, from NSMT-Te 1037 showing the long curved ascending branch along the intestine and large nephridial (anal) funnels extending towards the osophagus. Abbreviations: a, anus; ab, ascending branch; af, anal funnel; db, descending branch; es, oesophagus; in, intestine; lne, left nephridium; of, oral funnel; p, nephridiopore; rne, right nephridium.

Figure 7. Phoronopsis californica Hilton, 1930. A transverse section through the posterior part of the body, showing four mesenteries and the position of the giant nerve fibre, NSMT-Te 1038; B enlargement of transverse section showing longitudinal muscles and giant nerve fibre, NSMT-Te 1038; C transverse section through the basal part of lophophore showing top of the ascending branches of the nerphridia with the nephridiopore on the invagination of the collar fold, NSMT-Te 1037; D transverse section through the nephridium showing the nephridial funnel (oral funnel), NSMT-Te 1037; E upper part of nephridial funnel showing anal funnel, NSMT-Te 1037; F lower part of nephridial funnel showing oral funnel, NSMT-Te 1037. Abbreviations: ab, ascending branch; af, anal funnel; am, anal mesentery; in, intestine; llm, left lateral mesentery; lne, left nephridium; lnf, left giant nerve fibre; of, oral funnel; om, oral mesentery; p, nephridiopore; rlm, right lateral mesentery; rne, right nephridium; s, stomach. Scale bars: A = 500 μm; B = 100 μm; C, D = 300 μm; E, F = 200 μm.