from Korean Waters - Springer Link

Ocean Sci. J. (2010) 45(1):55-61 DOI 10.1007/s12601-010-0005-4

Note http://www.springer.com/12601

New Records of Three Paraprionospio Species (Polychaeta: Spionidae) from Korean Waters Hisashi Yokoyama1 and Jin-Woo Choi2*

National Research Institute of Aquaculture, Fisheries Research Agency, Minami-ise, Mie 516-0193, Japan South Sea Research Institute, KORDI, Geoje 656-830, Korea

1 2

Received 3 February 2010; Revised 7 March 2010; Accepted 22 March 2010 © KSO, KORDI and Springer 2010

Abstract − The spionid polychaete Paraprionospio pinnata (Ehlers 1901) has been widely reported from Korean waters. We examined some specimens belonging to the genus Paraprionospio that had been collected from Korean waters, and identified them as Paraprionospio coora Wilson, 1990, Paraprionospio cordifolia Yokoyama, 2007 and Paraprionospio patiens Yokoyama, 2007, which are new to the fauna of Korea. The present study suggests misidentification of the specimens that have been previously reported as P. pinnata from Korean waters. Key words − Paraprionospio, Spionidae, Polychaeta, taxonomy, Korea

1. Introduction The spionid polychaete, Paraprionospio pinnata, which was originally described by Ehlers (1901) based on specimens collected from Chile, has been regarded as a monotypic (Foster 1971) and cosmopolitan (Light 1978; Maciolek 1985) species. In Korean waters, this species was first reported from Suncheon Bay on the southern coast but as Prionospio pinnata (Paik 1972), and has been found at various sites in Korea (Hong and Lee 1983; Lim et al. 1992; Shin et al. 2001; Choi et al. 2005) as well as from Japanese waters (e.g. Imajima and Hartman 1964). Yokoyama and Tamai (1981), however, found that the Japanese specimens of Paraprionospio pinnata were comprised of four distinct forms of morphological variations based on a series of 11 characters. They suggested that the observed variations might be sufficient to allow the forms to be distinguished at the specific level, but they did not determine species names. *Corresponding author. E-mail: [email protected]

Later, Yokoyama (2007) published a revision of the genus Paraprionospio, in which 9 valid species including 4 Japanese species, that are P. coora Wilson, 1990 and 3 undescribed species (P. cordifolia Yokoyama, 2007, P. oceanensis Yokoyama, 2007 and P. patiens Yokoyama, 2007), were validated. Zhou et al. (2008) also examined Chinese specimens, which have been previously identified as P. pinnata, and found that they belong to the three species, P. coora, P. inaequibranchia (Caullery 1914) and an undescribed species P. cristata Zhou, Yokoyama and Li 2008. Yokoyama et al. (2010) reported the occurrence of P. coora, instead of P. pinnata, in the Mediterranean Sea. The above-mentioned studies indicate that the specimens previously reported as P. pinnata from the Far East and the Mediterranean Sea have been misidentified. Hence we examined some Paraprionospio specimens collected from Korean waters, and found that they agree with the descriptions of P. coora, P cordifolia and P. patiens, instead of P. pinnata.

2. Material and Methods Sampling data of Paraprionospio specimens used in the present study are summarized in Table 1. The specimens were collected by Jin-Woo Choi from Taean on the west coast of Korea and from 9 localities along the south coast including Gamak Bay, Sori-do, Gwangyang Bay, Seumjin River estuary, Masan Bay, Jinhae Bay, Okpo Bay, Busan Harbor and Ulsan Bay and from the shelf approximately 90 km off Ulsan (Fig. 1), at depths ranging from 5 m to 150 m between the years 2005 and 2009. All specimens were fixed with 4% formaldehyde buffered with sea water and

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Yokoyama, H. and Choi, J.-W.

Table 1. Sampling sites and number of individuals of the 3 Paraprionospio species examined in the present study Coordinates (N, E) Taean coast 36°56.20', 126°16.33' Taean coast 36°51.19', 126°10.62' Taean coast 36°47.17', 126°08.36' Taean coast 36°39.42', 126°16.39' Taean coast 36°26.18', 126°12.02' Taean coast 36°21.01', 126°12.01' Taean coast 36°21.25, 126°05.99' Sori-do coast 34°30.54', 127°48.06' Gamak Bay 34°44.25', 127°39.77' Gamak Bay 34°43.05', 127°39.18' Gamak Bay 34°43.06', 127°40.98' Gamak Bay 34°37.29', 127°42.34' Gwangyang Bay34°52.30', 127°39.47' Seumjin River 34°56.41', 127°46.31' estuary Masan Bay 35°10.64', 128°34.41' Masan Bay 35°10.83', 128°34.26' Masan Bay 35°08.63', 128°36.40' Masan Bay 35°08.44',128°36.32' Masan Bay 35°04.32', 128°39.09' Jinhae Bay 35°02.13', 128°37.47' Jinhae Bay 35°01.14', 128°35.38' Jinhae Bay 34°54.57', 128°36.06' Okpo Bay 34°53.07', 128°42.18' Okpo Bay 34°52.34', 128°42.02' Busan Harbor 35°07.05', 129°03.90' Busan Harbor 35°06.40', 129°03.12' Ulsan Bay 35°29.58', 129°23.48' Ulsan Bay 35°29.01', 129°24.01' Ulsan Bay 35°27.70', 129°25.48' Shelf off Ulsan 35°38.53', 129°50.29' Locality

Sampling Depth Sediment P. P. P. Habitat character date (m) type coora cordifolia patiens 2009/07/27 19 sand heavily impacted area by oil spill in 2007 1 2009/07/27 10 sand heavily impacted area by oil spill in 2007 2 2009/07/27 8 sand heavily impacted area by oil spill in 2007 1 2009/07/27 6 mud slightly impacted area by oil spill in 2007 3 2009/07/27 25 muddy sand moderately impacted area by oil spill in 2007 6 2009/07/27 21 muddy sand moderately impacted area by oil spill in 2007 2 2009/07/27 28 muddy sand moderately impacted area by oil spill in 2007 1 2007/04/27 20 sandy mud coast of an offshore island, oil spilled in 1995 1 2009/11/24 5 mud semi-enclosed bay, organically enriched 4 2009/07/20 9 mud semi-enclosed bay, organically enriched 1 2009/07/20 9 mud semi-enclosed bay, organically enriched 2 2009/07/20 10 mud semi-enclosed bay, organically enriched 4 2009/08/19 10-30 mud semi-enclosed bay, commercial pier, dredged 1 135 2009/11/10 10 sandy mud estuary, river mouth 1 2005/11/07 2006/05/22 2005/12/20 2006/03/24 2006/04/17 2007/08/27 2007/08/29 2007/08/28 2009/11/18 2009/11/18 2009/08/24 2009/02/26 2009/08/25 2009/08/25 2009/08/25 2007/04/09

10 9 10 20 15 20 20 15 20 15 12 11 7 18 36 150

mud mud mud mud mud mud mud mud mud mud mud mud sandy mud sandy mud sandy mud muddy sand

preserved in 70% ethanol. The body length and width of the 5th setiger (excluding parapodia) of worms were measured using an ocular micrometer. The specimens examined are deposited in the Library of Marine Sample of Korea Ocean Research and Development Institute (KORDI).

3. Taxonomic Account Paraprionospio coora Wilson, 1990 (Fig. 2) Paraprionospio coora Wilson, 1990; Yokoyama 2007, figure 8; Zhou et al. 2008; Yokoyama et al. 2010. Material examined 74 specimens collected from 9 localities on the west and

semi-enclosed bay, organically enriched semi-enclosed bay, organically enriched semi-enclosed bay, organically enriched semi-enclosed bay, organically enriched outfall of a sewage treatment plant tidal channel of embayment tidal channel of embayment semi-enclosed bay, organically enriched semi-enclosed bay, near a big shipyard semi-enclosed bay, organically enriched semi-enclosed, harbor semi-enclosed, harbor estuarine, river mouth, near shipyard estuarine, river mouth, near shipyard estuarine, river mouth, near shipyard continental shelf, dumping site

19 2 6

4 10

15 11 2 3 1 9 5 1 1 1 2

4

12 1 5

south coasts of Korea at depths ranging from 7 m to 150 m (Table 1). Description Largest complete specimen, 71 mm long, 1.9 mm wide with 114 setigers. Two pairs of black eyes on prostomium. Brown pigment patch usually present on lateral side of peristomium (Fig. 2). Small papilla on posterior margin of peristomium. Three pairs of branchiae on setigers 1–3. First and second pairs of branchiae approximately equal length, or first ones slightly longer than second ones. Third branchiae shortest. In basal region of first branchial shaft, 2–6 conic processes placed along anterior face. All branchiae bearing lamellar plates; in middle and distal regions, lamellae showing flabellate-shape (Fig. 2). A small

Paraprionospio (Polychaeta: Spionidae) from Korean waters

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Fig. 1. Map showing localities where the 3 Paraprionospio species were collected.

Fig. 2. Paraprionospio coora collected from Masan Bay. Anterior end, dorso-lateral view. Arrows indicate pigment patch and flabellateshaped lamellar plates of branchia.

protuberance usually present on dorsum near base of third branchiae. Neuropodial hooded hooks with 2–3 pairs of apical teeth above main fang from setiger 9, accompanied by alternating nonlimbate slender capillaries. Notopodial hooded hooks with 3 pairs of apical teeth above main fang

appearing between setigers 30 and 38. No ventral bilobed flap on setiger 8. Interneuropodial pouches present in approximately half of specimens examined (41 out of 74 specimens), appearing in setiger 8 or 9 and being indistinguishable between setigers 13 and 38. Membranous

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dorsal crests and semi-transparent dorsal cuticle absent. Pygidium with a long median anal cirrus and two short, lateral cirri. Distribution Western Japan, more southern than 37°N; Korea, Yellow Sea, East China Sea, New South Wales to Tasmania in Australia, Mediterranean. Remarks The Korean specimens of Paraprionospio coora closely agree with the original description of the species from Australia by Wilson (1990), but have 2–3 pairs of apical teeth in neuropodial hooded hooks rather than only 2 pairs of apical teeth. A variable number of apical teeth were noted within the specimens collected from Japanese waters (Yokoyama 2007), Chinese waters (Zhou et al. 2008) and the Mediterranean Sea (Yokoyama et al. 2010) suggesting that this is not a stable character to be used in distinguishing species. A small protuberance on the dorsum near the base of third branchiae was found in the Korean specimens as well as in Japanese and Mediterranean specimens (Yokoyama et al. 2010). Mediterranean specimens lacked interneuropodial pouches (Yokoyama et al. 2010). This character, however, was found in some Korean specimens similarly to the Japanese (Yokoyama 2007) and Chinese (Zhou et al. 2008) specimens, while most specimens collected from Australia had this character (Wilson 1990). Because the number of interneuropodial pouches varies from zero to about 30 even in local populations in Australia, China, Japan and Korea, this character is not dependable for distinguishing species.

Hence, we identified the Korean specimens as P. coora. P. coora can be differentiated from P. pinnata by the possession of a papilla on posterior margin of peristomium, pigment patches on peristomium, accessory processes on the first pair of branchiae and interneuropodial pouches and the absence of a semi-transparent dorsal cuticle. P. coora also differs from P. cordifolia and P. patiens by the absence of slender filaments on setiger 3 and semi-transparent dorsal cuticles. This is the first record of P. coora from Korean waters. Paraprionospio cordifolia Yokoyama, 2007 (Fig. 3) Paraprionospio cordifolia Yokoyama, 2007, figure 9. Material examined 146 specimens collected from 4 localities on the west and south coasts of Korea at depths ranging from 6 m to 30 m (Table 1). Description Largest complete specimen, 42 mm long, 0.94 mm wide with 96 setigers. Two pairs of black, small eyes in trapezoidal arrangement. A pair of yellowish-brown pigment patch usually visible between the two pairs of eyes. No papilla on posterior margin of peristomium. No pigment patch on peristomium. Three pairs of branchiae on setigers 1–3 bearing flabellate-shape lamellae (Fig. 3). Usually first pair longest, occasionally first and second pairs approximately equal length. Third pair shortest. A slender filament at base of third pair of branchiae. Anterior ventral margin in setiger

Fig. 3. Paraprionospio cordifolia collected from Okpo Bay. Anterior end, ventral view. Arrows indicate flabellate-shaped lamellar plates of branchia and ventral bilobed flap on setiger 8.


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8 protruding to form a bilobed membranous flap (Fig. 3); on 2 to 3 succeeding setigers anterior ventral margin projecting slightly. Interparapodial pouches absent except in one specimen collected from Okpo Bay having weak pouches from setiger 12. Membranous dorsal crests absent; instead, a faint ridge between both notopodial postsetal lamellae on setigers 21–36 present, accompanied by semi-transparent dorsal cuticle bearing circular convexities. Neuropodial hooded hooks with 3–4 pairs of apical teeth above main fang from setiger 9, accompanied by alternating nonlimbate slender capillaries. Notopodial hooded hooks with 2–3 pairs of apical teeth above main fang appearing from setiger 34–39. Pygidium with a long median anal cirrus and two short, lateral cirri.

possession of the ventral bilobed flap on setiger 8. This is the first record of P. cordifolia from Korean waters.

Remarks The Korean specimens of Paraprionospio cordifolia closely agree with the original description of the species from Japan by Yokoyama (2007), but have no interparapodial pouches except for one specimen collected from Okpo Bay. As noted in the remarks on P. coora, this character seems not dependable for distinguishing Paraprionospio species. Hence, we identified the Korean specimens as P. cordifolia. This species can be differentiated from P. pinnata by the possession of a slender filament at the base of pair of branchiae and a ventral bilobed flap on setiger 8. P. cordifolia also differs from P. coora and P. patiens by the

Description Largest complete specimen, 39 mm long, 0.96 mm wide with 99 setigers. Two pairs of black, small eyes in prostomium. Small papilla on posterior margin of peristomial wing. No pigment patch on peristomium. Three pairs of branchiae on setigers 1–3, bearing lamellae consisting of 2 plates, showing bifoliate-shape (Fig. 4). First and second pairs of branchiae approximately equal length, or first ones slightly longer than second ones. Third branchiae shortest. A slender filament at the base of third pair of branchiae. Ventral bilobed flap absent. Interparapodial pouches absent. Notopodial postsetal lamellae united across dorsum, forming dorsal crests on setigers 21–35,

Distribution Western Japan, more southern than 36°N; Korea; East China Sea; Hong Kong. Paraprionospio patiens Yokoyama, 2007 (Fig. 4) Paraprionospio patiens Yokoyama, 2007, figures 14, 15. Material examined 59 specimens collected from 5 localities on the south coast in Korea at depths ranging from 5 m to 20 m (Table 1).

Fig. 4. Paraprionospio patiens collected from Masan Bay. Anterior end, dorso-lateral view. Arrow indicates bifoliate-shaped lamellar plates of branchia.

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accompanied by semi-transparent dorsal cuticle bearing circular convexities. Among 59 specimens examined, only one specimen having dorsal crests and semi-transparent dorsal cuticle on setigers 22−36. Neuropodial hooded hooks with 3–4 apical teeth above main fang and alternating capillaries appearing from setiger 9. Neuropodial capillaries short and limbate on setiger 9, replaced by long, fine, nonlimbate capillaries from setiger 10. Notopodial hooded hooks with 3 apical teeth from setiger 32–35. Pygidium with a long median anal cirrus and two short, lateral cirri. Remarks Paraprionospio patiens can be differentiated from P. pinnata by the possession of a papilla on posterior margin of peristomium, bifoliate lamellae of branchiae instead of flabellate ones, a slender filament at the base of 3rd branchiae, dorsal crests on setigers 21–35 and short and limbate neuropodial capillaries on setiger 9. P. patiens also differs from P. cordifolia and P. coora by the possession of the bifoliate lamellae of branchiae. This is the first record of P. patiens from Korean waters. Distribution Western Japan, more southern than 37°N; Korea; Indonesia.

4. Concluding Remarks Paraprionospio pinnata has been reported from various areas of Korean waters (Paik 1972; Hong and Lee 1983; Lim et al. 1992; Ma et al. 1995; Lim and Hong 1997; Paik and Yun 2000; Shin et al. 2001; Choi et al. 2005; Yoon et al. 2009). We examined the material from the southern and western coasts of Korea. None of these specimens was identified as P. pinnata; they were identified as P. coora, P. cordifolia and P. patiens. Similar taxonomic confusion had been reported from Japan and China. Yokoyama (2007) found the same 3 Paraprionospio species and P. oceanensis from Japanese coastal waters. Zhou et al. (2008) reported P. coora, P. inaequibranchia and P. cristata from Chinese waters. They suggested misidentification of the specimens that were previously reported as P. pinnata from China. The present examination of the Korean specimens suggests that P. pinnata is not distributed in the Far East. The present study revealed a close similarity in the fauna of Paraprionospio between Korea and Japan. Of 4 species reported from Japan, 3 species including P. coora, P.

cordifolia and P. patiens were found in the Korean fauna. In Japan, P. patiens is known as a biological indicator of heavy organic pollution and/or oxygen-depleted waters, and P. cordifolia is known as an indicator of semi-enclosed, eutrophicated environments (Tamai 1981). On the other hand, P. coora occurs not only on mud bottoms in coastal bays but also on the shelf as well as on sandy bottoms that face open water (Tamai 1981). A similar pattern of distribution was also found in Korea. That is, P. patiens was collected from organically enriched, mud bottoms in Gamak, Masan and Okpo bays, while P. cordifolia inhabited mud bottoms in semi-enclosed bays such as Gwangyang, Gamak and Okpo bays and the Taean coastal area (Table 1). On the other hand, P. coora showed a wide range of distribution including estuaries and semi-enclosed bays that were occasionally impacted by organic enrichment and/or oil spill (Taean coast, Gwangyang Bay, Masan Bay, Jinhae Bay, Okpo Bay, Busan Harbor and Ulsan Bay), coastal area that faces toward open water (Sorido coast) and the shelf off Ulsan. This species occurred in all sediment types including mud (Gamak Bay, Gwangyang Bay, Masan Bay, Jinhae Bay, Okpo Bay and Busan Harbor), sandy mud (Ulsan Bay, Sori-do coast and Gwangyang Bay), muddy sand (Taean coast, shelf off Ulsan) and sand (Taean coast). As the favorable habitat is different between the 3 Paraprionospio species, the correct identification of species, therefore, is essential for the evaluation of the coastal environment using these species as a biological indicator. The follow is an identification key to the 3 Korean species of Paraprionospio. KEY TO KOREAN SPECIES OF PARAPRIONOSPIO 1a. Ventral bilobed flap on setiger 8 ········································· Paraprionospio cordifolia 1b. Ventral bilobed flap absent····································· 2 2a. Brown pigment patch usually present on lateral side of peristomium. Filaments on dorsum of setiger 3 absent. Conic processes in basal region of 1st branchia. Branchial lamellae flabellate. Neuropodial capillaries on setiger 9 long, non-limbate. Membranous dorsal crests and semi-transparent dorsal cuticles absent ················································Paraprionospio coora 2b. Brown pigment patch absent. Filaments on dorsum of setiger 3. Conic processes absent from basal region of 1st branchia. Branchial lamellae bifoliate. Neuropodial


capillaries on setiger 9 short, limbate. Membranous dorsal crests and semi-transparent dorsal cuticles from setiger 21 ··············································Paraprionospio patiens

Acknowledgements We are grateful to Prof. H. Tsutsumi of the Prefectural University of Kumamoto for providing the camera system which was used to take photographs of the specimens. The specimen collection was possible by the grants from KORDI (PE98313) and by research fund from the Korean Ministry of Land, Transport and Maritime Affairs (PM55020: Oil Spill Environmental Impact Assessment and Environmental Restoration).

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