Lernaeenicus ramosus from the Amakusa-nada Sea Biogeography 19. 85–92. Sep. 20, 2017

First records of the acropomatid fish (Teleostei: ) Parascombrops yamanouei from Japan and the Philippines

Kyoji Fujiwara1*, Ulysses B. Alama2, Makoto Okamoto3 and Hiroyuki Motomura4

1 Graduate School of Fisheries, Kagoshima University, 4-50-20 Shimoarata, Kagoshima 890-0056, Japan 2 Museum of Natural Sciences, College of Fisheries and Ocean Sciences, University of the Philippines Visayas, 5023 Miagao, Iloilo, Philippines 3 Marine Fisheries Research and Development Center (JAMARC) of Fisheries Research Agency, 15F Queen's Tower B, 2-3-3 Minatomirai, Nishiku, Yokohama, Kanagawa 220-6115, Japan 4 The Kagoshima University Museum, 1-21-30 Korimoto, Kagoshima 890-0065, Japan

Abstract. Two examples (43.6 and 103.4 mm standard length) of Parascombrops yamanouei Schwarzhans, Prokofiev & Ho, 2017, recently described from 28 specimens from Taiwan and the Timor Sea, are recorded from Japan and the Philippines, the smaller specimen (from Japan) representing the northernmost record of the species. The two specimens are described in detail and comparisons made with congeners.

Key words: range extension, distribution, East China Sea, Panay Island, northernmost record.

Introduction Schwarzhans, Prokofiev & Ho, 2017, a species pre- viously known only from Taiwan and the Timor Sea The acropomatid fish Parascombrops (Schwarzhans & Prokofiev 2017). These specimens Alcock, 1889, previously regarded as synonym of are described herein, being the first records of P. Synagrops Günther, 1887, was recently reinstated yamanouei from Japan and the Philippines. by Schwarzhans & Prokofiev (2017), who recog- nized 13 species, including seven new species, in Materials and Methods the genus. Parascombrops is characterized by the following combination of characters: 9 first dorsal- Counts and measurements followed Hubbs & fin spines, II, 7 or III, 6 anal-fin rays, teeth on the -ec Lagler (1958) and Schwarzhans & Prokofiev (2017). topterygoids, eighth interneural gap vacant, serrated Measurements were made to the nearest 0.1 mm pelvic-fin spine, abdominal luminous organ absent, with calipers. Standard length is expressed as SL. and pre-dorsal formula /0+0/0+2/ (Schwarzhans & Curatorial procedures followed Motomura & Ishi- Prokofiev 2017). kawa (2013). Institutional codes used in this study During examination of specimens of Parascom- include KAUM (Kagoshima University Museum, brops collected from Japan and the Philippines, two Kagoshima, Japan) and UPVMI (Museum of Natu- specimens (43.6 and 103.4 mm standard length) ral Sciences, University of the Philippines Visayas, were identified as Parascombrops yamanouei Miagao, Iloilo, Philippines). ——————————————————————— *Corresponding author: [email protected]

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Parascombrops Alcock, 1889 Material examined. JAPAN: KAUM–I. 81502, [New Japanese name: Himesumikuiuo zoku] 43.6 mm SL, East China Sea, 30°15′N, 124°15′E, 57–58 m depth, bottom trawl, 8 December 2015. Parascombrops yamanouei Schwarzhans, PHILIPPINES: KAUM–I. 69404, 103.4 mm SL, Prokofiev & Ho in Schwarzhans & Prokofiev, 2017 off Miagao, Panay Island, 10°37′N, 122°14′E, 24 [New English name: Yamanoue’s Seabass; new Japa- February 2015. nese name: Sedaka-himesumikuiuo] Description. Counts and measurements given in (Figs. 1–4, Table 1) Table 1. Body moderately elongate, laterally com- pressed (Fig. 1); body depth 3.11–3.24 in SL. Dorsal Parascombrops yamanouei Schwarzhans, Prokofiev profile of head strongly convex. Snout with pointed & Ho in Schwarzhans & Prokofiev, 2017: 50, figs. profile. Orbit diameter 2.65–3.15 in head length. 7M, 10F, 13M, 15S–U, 30, 35 (original descrip- Snout length 62–73% of orbit diameter. Anterior tion; type locality: Dong-gang, Pingtung, Taiwan; nostril opening elliptical; posterior nostril opening paratype localities: Dong-gang, Pingtung, Taiwan; slit-like, located on anterior margin of orbit. Interor- Timor Sea). bital space strongly convex. Mouth large, oblique;

Fig. 1. Fresh specimens of Parascombrops yamanouei. (A) KAUM–I. 81502, 43.6 mm SL, East China Sea, Japan; (B) KAUM–I. 69404, 103.4 mm SL, off Miagao, Panay Island, Philippines.

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Fig. 2. Radiographs of the first anal-fin pterygiophores in Parascombrops yamanouei. (A) KAUM–I. 81502, 43.6 mm SL, East China Sea, Japan; (B) KAUM–I. 69404, 103.4 mm SL, off Miagao, Panay Island, Philippines.

Fig. 3. Distributional records of Parascombrops yamanouei. Star, and open and closed circles indicate type locality, paratype locality and new records in this study, respectively.

Fig. 4. Relationship of orbit diameter (% standard length; SL) to SL (mm) in (A) Parascombrops yamanouei and (B) Parascombrops philippinensis.

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Table 1. Counts and proportional measurements, expressed as percentages of standard length, of specimens of Parascombrops yamanouei and P. philippinensis. Modes and means in parentheses.

P. yamanouei P. philippinensis Schwarzhans & This study a This study Prokofiev (2017) Japan Philippines Taiwan Taiwan Japan n = 1 n = 1 n = 3 n = 28 n = 15 Standard length (mm; SL) 43.6 103.4 87.7–89.5 64–109 33.6–65.6 Counts Dorsal-fin rays IX-I, 9 IX-I, 9 IX-I, 9 IX-I, 9 IX-I, 9 Anal-fin rays II, 7 II, 7 II, 7 II, 7 II, 7 Pectoral-fin rays 15 16 15 14–15 (15) 14–16 (15) Gill rakers on 1st gill arch 15 15 15 13–16 (15) 15–18 (16) Pseudobranchial filaments 18 23 20–23 (23) 18–27 (21) 14–21 (15)e Pored lateral-line scales broken 28 27–28 (28) – 27–29 (28)f Measurements (% SL) Head length 40.4 39.0 38.0–38.5 (38.3) 34.4–41.2 (38.3)b 35.1–39.2 (37.5) Postorbital length 16.3 19.0 18.1–20.1 (19.0) – 15.3–19.2 (17.5) Body depth 32.1 30.9 33.2–35.9 (34.9) 28.0–33.9 (31.5)c 22.0–25.1 (23.8) Body width 16.3 15.5 14.2–15.6 (15.0) – 12.3–14.9 (13.5) Snout length 8.5 9.0 8.4–8.9 (8.7) 8.7–10.4 (9.4)b 7.9–9.7 (8.6) Upper-jaw length 18.6 17.8 16.5–17.8 (17.1) – 15.4–17.2 (16.1) Orbit diameter 13.8 12.4 12.3–12.5 (12.5) 10.2–12.8 (11.9) 12.1–13.8 (12.9) Interorbital width 8.9 9.0 8.4–9.2 (8.7) – 9.1–9.9 (9.4) Pre-1st dorsal-fin length 41.3 40.1 38.4–40.2 (39.4) 37.9–42.2 (39.8)d 37.2–39.8 (38.5) Pre-2nd dorsal-fin length 67.2 69.3 67.7–70.9 (69.0) – 63.1–66.2 (64.9) Pre-anal-fin length 70.0 69.9 72.0–73.7 (73.0) 64.9–73.4 (69.3)d 64.8–68.2 (66.4) Pre-pectoral-fin length 38.8 37.5 36.3–37.9 (36.8) – 34.9–38.7 (36.2) Pre-pelvic-fin length 42.0 39.7 39.0–41.3 (40.1) – 35.2–38.1 (36.4) 1st dorsal-fin base length 22.0 22.9 21.2–24.2 (22.6) – 17.8–20.7 (19.7) 2nd dorsal-fin base length 16.1 13.8 13.1–14.2 (13.7) – 12.7–15.3 (14.0) Anal-fin base length 11.9 11.1 11.1–11.5 (11.3) – 11.4–14.3 (12.5) Caudal-peduncle length 22.2 23.0 20.0–22.0 (20.8) – 23.0–25.1 (23.8) Caudal-peduncle depth 11.7 12.4 11.2–13.4 (12.3) – 9.1–10.3 (9.7) Pectoral-fin length 25.2 26.5 25.7–27.9 (26.6) 23.5–26.6 (25.1) 22.6–27.9 (25.0) Pelvic-fin length broken 20.8 22.3–22.7 (22.5) – 14.5–19.9 (17.4) a including type specimens; b–f based on 22, 26, 23, 14, and 11 specimens respectively. maxilla expanded posteriorly, posterior margin Palatines narrow, anteriorly with 1 or 2 longer teeth, slightly beyond level with anterior margin of pupil. thereafter with 1 or 2 rows of granular teeth; ec- Tip of lower jaw protruding anteriorly beyond upper topterygoids wide, with 3–6 rows of granular teeth. jaw. Caudal-peduncle length and depth 1.64–1.69 Tongue without tooth patch. and 3.12–3.15 in head length, respectively. Posterior margin of lower subopercle and interop- Upper and lower jaw with a pair of canine teeth ercle weakly serrated or smooth. Preopercular lobe near symphysis, followed posteriorly by a wide band without longitudinal ridges, a small spike present of minute granular teeth. Lower jaw with 3 or 4 ca- (in KAUM–I. 81502); denticles of serrated posterior nine teeth on each side. Vomer with V-shaped tooth margin somewhat extended, forming crests on pre- patch with reduced dentition (very few granular teeth opercular lobe; inner edge of preopercle with 3–5 anteriorly, 1 or 2 long conical teeth posterolaterally). small denticles not extending along ventral branch.

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Only pelvic-fin spine serrated. Pectoral-fin rays ectopterygoids wide, with 3–6 rows of granular branched without upper most ray; third or fourth teeth; tongue without tooth patch; preopercular lobe pectoral-fin ray longest, not reaching anal-fin inser- without longitudinal ridges (but with a small spike tion. Anal fin short; first anal-fin spine very short; in KAUM–I. 81502); pelvic-fin spine serrated; pos- first or second anal-fin soft ray longest. Caudal fin terior tip of pectoral fin not reaching vertical through forked. anal-fin origin; abdominal luminous organ absent; Scales cycloid, deciduous; head, including max- first anal-fin pterygiophore relatively short, straight. illa and snout, naked. Lateral line complete. Gill rak- However, some morphometrics and meristics of ers long, slender. Abdominal luminous organ absent. the former specimens differed slightly from those First anal-fin pterygiophore relatively short, straight given by Schwarzhans & Prokofiev (2017): e.g., 1 (Fig. 2). Pre-dorsal formula /0+0/0+2/. Vertebrae or 2 long conical teeth posterolaterally on the vomer 9+15. [vs. 1 tooth in Schwarzhans & Prokofiev (2017)]; Coloration when fresh (Fig. 1B). Body dark pectoral-fin rays 16 (vs. 14 or 15; Table 1); and snout brown dorsally, silvery-white ventrally. Anterior length 8.5% SL (vs. 8.7–10.4% SL; Table 1). These portion of dorsal and caudal fins brownish. Pectoral- minor differences were regarded as interspecific fin base and upper portion of pectoral fin slightly variation, the snout length proportion being within brownish. Lower portion of pectoral, pelvic and anal the range of three Taiwanese specimens (8.4–8.9% fins translucent. SL) examined in this study (Table 1). Orbit diameter Coloration when preserved (Fig. 1A). Body pale of the Japanese specimen (13.8% SL) was much brown. Dorsal surface of head, lower jaw tip, and greater than the range of the type specimens given in scale pockets above lateral line with numerous small the original description (10.2–12.8% SL), the Philip- diffuse dotted melanophores; body similar, melano- pine specimen (12.4% SL), and additional Taiwanese phores concentrated along posterior half of scale specimens examined (12.3–12.5% SL) (Table 1). pockets. Such a size difference probably represents ontoge- Distribution and habitat. Parascombrops yaman- netic change, the Japanese specimen (43.6 mm SL) ouei is known only from the East China Sea (Japan), being much smaller than the others (64–109 mm Taiwan, Panay Island (Philippines) and the Timor SL; Table 1, Fig. 4A). Similar ontogenetic change in Sea (Schwarzhans & Prokofiev 2017; this study: Fig. orbit diameter was confirmed in the specimens of P. 3). The type specimens of P. yamanouei were col- philippinensis examined in this study (Fig. 4B). lected in depths of about 80–100 m (Schwarzhans Parascombrops yamanouei differs from its con- & Prokofiev 2017) and the Japanese specimen from geners, except for P. analis (Katayama, 1957), P. 57–58 m. Collection depth of the Philippine speci- madagascariensis Schwarzhans & Prokofiev, 2017 men (purchased at a fish market) is unknown. and P. serratospinosus (Smith & Radcliffe, 1912), Remarks. The two specimens from Japan and the in having greater body depth [>30% SL (mean)] Philippines agree closely with the original descrip- (Schwarzhans & Prokofiev 2017). Parascombrops tion of Parascombrops yamanouei Schwarzhans, yamanouei is distinct from P. analis and P. ser- Prokofiev & Ho, 2017, having 9 first dorsal-fin ratospinosus in having II, 7 anal-fin rays (vs. III, 6 spines; II, 7 anal-fin rays; 15 gill rakers; body depth in P. analis) and only the pelvic-fin spine serrated 30.9–32.1% SL; 3 or 4 canine teeth on each side of (vs. dorsal-, anal-, and pelvic-fin spines serrated inP. the lower jaw; vomer with V-shaped tooth patch; serratospinosus) (Schwarzhans & Prokofiev 2017;

− 89 − First records of the acropomatid fish (Teleostei: Perciformes) Parascombrops yamanouei from Japan and the Philippines Kyoji Fujiwara, Ulysses B. Alama, Makoto Okamoto and Hiroyuki Motomura this study). Although P. yamanouei is most similar 27.8% SL); 3 canine teeth on each side of lower jaw; to P. madagascariensis known only from Mada- V-shaped tooth patch on vomer; preopercular lobe gascar and Réunion, the former is distinguished by without longitudinal ridges; snout length ca. 70% 1 or 2 long conical teeth posterolaterally on the V- of orbit diameter (estimated from sketch); pelvic-fin shaped vomerine tooth patch (vs. continuous row of spine only serrated; posterior tip of pectoral fin not long conical teeth absent on triangular tooth patch in reaching to anal-fin origin]. Reports on P. philippin- P. madagascariensis), 3–6 rows of granular teeth on ensis from Japan by Mochizuki (1984), Yamakawa each ectopterygoid (vs. 1 or 2 rows), preopercle usu- (1985), Yamada (1986), Hatooka (1993, 2013) and ally with a small spike (vs. always without spikes), Yamada et al. (2007) are similarly confirmed here and the first anal-fin pterygiophore somewhat short as P. philippinensis. However, a single specimen and straight (vs. long and slightly bent toward tip) (UPVMI 1615, 140.3 mm SL) from the Philippines (Schwarzhans & Prokofiev 2017; this study). reported as P. philippinensis by Okamoto (2017), Among the shallow body depth species [less than was here identified as P. analis (Katayama, 1957), 30% SL (mean)] of Parascombrops, P. philippinen- characterized by the following characters: 9 first sis (Günther, 1880) and P. nakayamai Schwarzhans dorsal-fin spines; III, 6 anal-fin rays; 17 gill rakers; & Prokofiev, 2017 are similar to P. yamanouei in body depth 31.1% SL, and pelvic-fin spine only ser- sharing the following combination of characters: rated. Although UPVMI 1615 possesses 35 pseudo- 2–4 canine teeth on each side of lower jaw; tongue branchial filaments, Schwarzhans & Prokofiev (2017) without tooth patch; preopercular lobe without lon- noted counts of 16–23 for the species. The difference gitudinal ridges; pelvic-fin spine only serrated; and probably represents ontogenetic change, UPVMI posterior tip of pectoral fin not reaching to anal-fin 1615 (140.3 mm SL) being much larger than the origin (Schwarzhans & Prokofiev 2017; this study). specimens examined by Schwarzhans & Prokofiev In addition to body depth difference, P. yamanouei (2017) (29.0–107.5 mm SL). Those authors noted, in differs from the other two species in having 3–6 fact, that the number of pseudobranchial filaments in rows of granular teeth on each ectopterygoid (vs. 1 P. analis increases with growth. or 2 rows in P. philippinensis), a somewhat larger Parascombrops yamanouei has previously been body size [>100 mm SL (vs. ca. 80 mm SL)], snout recorded only from Taiwan and the Timor Sea, the length 62–91% of orbit diameter (vs. 87–113% in P. present specimens from the East China Sea and Pa- nakayamai), and 14–16 gill rakers (vs. 11–14 in P. nay Island representing the first records of P. yaman- nakayamai) (Schwarzhans & Prokofiev 2017; this ouei from Japan and the Philippines, respectively, study). the Japanese specimen also being the northernmost Since P. yamanouei has previously been identified record for the species. Although the species was as P. philippinensis (see Schwarzhans & Prokofiev previously considered to have an antitropical dis- 2017), previous records of P. philippinensis from tribution (Taiwan and Timor Sea) (Schwarzhans & Japan and the Philippines were also examined. Par- Prokofiev 2017), the Philippines record suggests oth- ascombrops philippinensis was initially recorded erwise, although the distribution may be antiequato- from Japan by Katayama (1960), whose description rial. and sketch are here confirmed as representing true P. The new Japanese names “Himesumikuiuo-zoku” philippinensis [9 first dorsal-fin spines; II, 7 anal-fin and “Sedaka-himesumikuiuo” are proposed for the rays; 17–18 gill rakers; shallow body depth (23.2– genus Parascombrops and P. yamanouei (based on

− 90 − First records of the acropomatid fish (Teleostei: Perciformes) Parascombrops yamanouei from Japan and the Philippines Kyoji Fujiwara, Ulysses B. Alama, Makoto Okamoto and Hiroyuki Motomura

KAUM–I. 81502), respectively. tablishment of Research and Education Network on Comparative material examined. Parascombrops Biodiversity and Its Conservation in the Satsunan analis: UPVMI 1615, 140.3 mm SL, Panay Island, Islands” project of Kagoshima University adopted Philippines. Parascombrops nakayamai: KAUM–I. by the Ministry of Education, Culture, Sports, Sci- 80885, 103.0 mm SL, Panay Island, Philippines. Par- ence and Technology, Japan. The study was con- ascombrops philippinensis: KAUM–I. 1472, 50.3 mm ducted under a Memorandum of Agreement for joint SL, KAUM–I. 3941, 65.6 mm SL, KAUM–I. 5177, research made by and among the Department of 47.0 mm SL, KAUM–I. 10422, 50.0 mm SL, KAUM– Agriculture of the Republic of the Philippines (DA), I. 17594, 47.5 mm SL, KAUM–I. 17612, 54.9 mm SL, the University of the Philippines Visayas (UPV), the KAUM–I. 17743, 43.5 mm SL, KAUM–I. 17814, 53.7 Kagoshima University Museum, the Research Insti- mm SL, KAUM–I. 25210, 47.5 mm SL, KAUM–I. tute for Humanity and Nature, and Tokai University, 28307, 48.4 mm SL, KAUM–I. 44875, 33.6 mm SL, facilitated by S. Sanchez [Bureau of Fisheries and KAUM–I. 63203, 53.5 mm SL, KAUM–I. 71249, 56.4 Aquatic Resources (BFAR), DA]. P. Alcala (DA) mm SL, KAUM–I. 98168, 50.3 mm SL, Kagoshima, provided a Prior Informed Consent Certificate, and Japan; KAUM–I. 75363, 57.2 mm SL, East China Sea, I. Cabacaba and S. Nolasco (BFAR, DA) provided a Japan. Parascombrops serratospinosus: KAUM–I. fish specimen Export Certificate (No. 2016-39812). 150366, 61.1 mm SL, Pingtung, Taiwan. Parascom- We thank the staff of the Office of the Vice-Chan- brops yamanouei: KAUM–I. 44626, 87.7 mm SL, cellor for Research and Extension, UPV, and UPV KAUM–I. 44627, 89.5 mm SL, Kaohsiung, Taiwan; Museum of Natural Sciences, College of Fisheries, KAUM–I. 44829, 89.4 mm SL, Yilan, Taiwan. UPV, including R. Babaran, S. Garibay, V. Urbina, L. Mooc, C. Rubido, E. Abunal, A. Guzman, R. Cruz, A. Acknowledgments Gaje, and R. Traifalgar, and graduate students of the College of Fisheries, UPV for their support of this We are especially grateful to M. Matsunuma research collaboration. (Kochi University, Japan), K. Koeda (National Mu- seum of Marine Biology and Aquarium, Taiwan), T. References Yoshida and H. Hata (KAUM) for providing litera- ture, H. Senou (Kanagawa Prefectural Museum of Hatooka, K., 1993. Percichthyidae. In Nakabo, T. Natural History, Japan) for his assistance in taking (Ed.), Fishes of Japan with Pictorial Keys to the x-rays, Y. Haraguchi (KAUM) and other volunteers Species, First Edition: 594–599, 1305. Tokai Uni- and students of KAUM for curatorial assistance, versity Press, Tokyo (In Japanese). and G. Hardy (Ngunguru, New Zealand) for read- Hatooka, K., 2013. . In Nakabo, T. ing the manuscript and providing help with English. (Ed.), Fishes of Japan with Pictorial Keys to the This study was supported in part by JSPS KAK- Species, Third Edition: 750–753, 1958–1959. ENHI Grant Numbers JP19770067, JP26241027, Tokai University Press, Hadano (In Japanese). JP24370041, JP23580259, and JP26450265; the Hubbs, C. L. & Lagler, K. F., 1958. Fishes of the JSPS Core-to-Core Program: B Asia-Africa Science Great Lakes Region. University of Michigan Platforms; the “Biological Properties of Biodiversity Press, Ann Arbor. Hotspots in Japan” project of the National Museum Katayama, M., 1960. Fauna Japonica: Serranidae of Nature and Science, Tsukuba, Japan; and “Es- (Pisces). Biogeographical Society of Japan, To-

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kyo. bilitation and revision of Parascombrops Alcock, Mochizuki, K., 1984. Synagrops philippinensis. In 1889 including description of seven new species Masuda, H., Amaoka, K., Araga, T., Ueno, T. & and two new genera (Perciformes: Acropomati- Yoshino, T. (Eds.), The Fishes of the Japanese dae). Zootaxa, 4260: 1–74. Archipelago First Edition: 122, pl. 110-B. Tokai Yamada, U. 1986. Synagrops phillipinensis University Press, Tokyo (In Japanese). (Günther). In Okamura, O. (Ed.), Fishes of the Motomura, H. & Ishikawa, S. (Eds.), 2013. Fish East China Sea and the Yellow Sea: 138. Seikai Collection Building and Procedures Manual. Eng- Regional Fisheries Research Laboratory, Nagasaki lish Edition. The Kagoshima University Museum, (In Japanese). Kagoshima and the Research Institute for Human- Yamada, U., Tokimura, M., Horikawa, H. & Nakabo, ity and Nature, Kyoto. T. 2007. Fishes and Fisheries of the East China Okamoto, M., 2017. Parascombrops philippinensis. and Yellow Seas. Tokai University Press, Hadano In Motomura, H., Alama, U. B., Muto, N., Ba- (In Japanese). baran, R. P. & Ishikawa, S. (Eds.), Commercial Yamakawa, T., 1985. Synagrops philippinensis. In and Bycatch Market Fishes of Panay Island, Okamura, O. (Ed.), Fishes of the Okinawa Trough Republic of the Philippines: 79. The Kagoshima and the Adjacent Waters II: 458–459, 663. Japan University Museum, Kagoshima, University of Fisheries Resource Conservation Association, To- the Philippines Visayas, Iloilo, and Research In- kyo (In Japanese). stitute for Humanity and Nature, Kyoto. Schwarzhans, W. W. & Prokofiev, A. M., 2017. Re- appraisal of Synagrops Günther, 1887 with reha- (Received June 21, 2017; Accepted September 8, 2017)

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