Pseudopolydora achaeta Radashevsky & Hsieh, 2000

Radashevsky, Vasily I., Malyar, Vasily V. & Pankova, Victoria V., 2024, Cryptic invasions of Pseudopolydora (Annelida: Spionidae), with description of a new species from Queensland, Australia, Zootaxa 5486 (2), pp. 213-240 : 219-222

Pseudopolydora achaeta Radashevsky & Hsieh, 2000

Figures 2–4 , 6A, B

Pseudopolydora achaeta Radashevsky & Hsieh, 2000b: 223−226 , figs 4, 5, 11A. Lana et al. 2006: 50. Junqueira et al. 2009: 209–212, textfig. Moshchenko & Belan 2010: 275. Zvyagintsev et al. 2011: 53. Bogantes et al. 2021: 581, fig. 2A, B. Radashevsky et al. 2021a: 128–130, fig. 3.

Pseudopolydora sp. A : Radashevsky & Migotto 2006: fig. 1C.

Not Pseudopolydora achaeta : Abe et al. 2014: 3−5; 2016: 654−656, fig. 3; 2019: 6−11.

Not Pseudopolydora aff. achaeta : Abe & Sato-Okoshi 2021: 56−57, fig. 9A, B (larval morphology).

Type material examined. Taiwan: Tainan Co., South China Sea, Tsengwen River estuary, 23.067ºN, 120.083ºE, <2 m, mud, coll. Hsieh H.-L., 18 October 1994, ASIZ W-121 (holotype) . ASIZ W-113–120 , W-122–143 (676 paratypes); IBMV 3401 (135 paratypes); USNM 186524–186526 (458 paratypes) .

Other material examined. Brazil, Paraná: MIMB 40945 (1); MZUSP 237, 240 (23); VIR 19358 (1); São Paulo: MZUSP 236, 239 (27).

Kuwait, Arabian Gulf: MIMB 40934 (2).

Martinique, Caribbean Sea: MIMB 40944 (7).

Russia, Sea of Japan: MIMB 4015 (4), 4016 (1), 40935 (1); VIR 700 (1).

South Korea, East Sea: MIMB 40936–40943 (14).

Taiwan, South China Sea: MIMB 40923 (29).

Vietnam, Nha Trang Bay: MIMB 40946 (1), 42751 (1); VIR 13861 (2), 25357 (2).

Full information about the samples is given in the Supplementary Table S1 .

Adult diagnostic characters. Adults up to 25 mm long, 1.5 mm wide for 95 chaetigers. Paired transverse bands of black pigment on dorsal and ventral sides of 10−16 anterior chaetigers; small median dorsal melanophores from chaetigers 3–6 to chaetigers 10–16 ( Fig. 2A, B ). Prostomium anteriorly weakly incised, notched or almost blunt, posteriorly extending to end of chaetiger 2 as a low caruncle ( Fig. 6A ). Lateral lips of peristomium forming conspicuous transverse fold along midline of ventral and lateral sides of head. Occipital antenna present. Two pairs of black eyes usually present. Chaetiger 1 reduced, weakly separated from peristomium, without notochaetae, with short fine capillaries in neuropodia; small notopodial and well developed neuropodial lamellae present. Chaetiger 4 with anterior-row notochaetae of intermediate shape between winged capillaries of chaetiger 3 and pennoned spines of chaetiger 5; posterior-row notochaetae slender capillaries, same as on chaetiger 3 ( Fig. 3A ). Chaetiger 5 same in size as chaetigers 4 or 6, with postchaetal lamellae in both rami; dorsal superior and ventral capillaries same in size and number as those chaetae on chaetigers 4 or 6; two kinds of heavy spines in notopodia arranged in a straight or slightly curved vertical double row: anterior-row spines pennoned, with curved pointed tip; posterior-row spines simple falcate ( Fig. 3B ). Posterior notopodia with only slender capillaries. Bidentate hooded hooks in neuropodia from chaetiger 8, up to 16 in a series ( Fig. 3C ). Branchiae from chaetiger 7, up to 15 pairs ( Fig. 6A ). Pygidium flaring disc with wide dorsal gap and one pair of dorso-lateral processes. Glandular pouches in neuropodia from chaetiger 1, largest and double in each neuropodium in chaetigers 6 and 7, single in other neuropodia. Digestive tract without gizzard-like structure. Nephridia from chaetiger 4 onwards.

Habitat. Adult P. achaeta live in silty tubes in muddy sand intertidally and in shallow water. The tubes are up to 70 mm long, 3 mm wide, and protrude above the sediment up to 5 mm. The population density in some local places (for example, in Taiwan) reaches thousands of individuals per 1 m 2.

Reproduction. Pseudopolydora achaeta is dioecious. Both females and males become mature after growing to about 10 mm long with 50–60 chaetigers. Of 60 examined mature individuals, 27 were females and 33 were males. Gametes develop from chaetigers 18–20 (usually from chaetiger 19) to chaetigers 36−53 ( Fig. 6B ). Paired testes or ovaries are attached to segmental blood vessels in fertile chaetigers.

Larval morphology. Pelagic larvae of P. achaeta measured up to 1.6 mm long with 25 chaetigers were collected from Paranaguá Bay (Paraná, Brazil), São Sebastião Channel (São Paulo, Brazil), Peter the Great Bay ( Sea of Japan, Russia), and from Nha Trang Bay ( South China Sea , Vietnam). The larvae from different regions were similar to each other. The smallest newly settled juvenile from Paranaguá Bay was about 600 µm long with 16 chaetigers. The larva described below and illustrated was collected from Nha Trang Bay in May 2022.

The 20-chaetiger larva about 1.1 mm long ( Fig. 4A–D ). Yellow pigment present on prostomium, in lateral lips of peristomium, on dorsal and ventral sides of chaetigers, and on ventral side of pygidium. Small melanophores in lateral lips of peristomium. Large middorsal melanophore on chaetiger 1. Small paired dorsal melanophores and unpaired middorsal vesiculate melanophores from chaetiger 3 onwards. Dorso-lateral melanophores from chaetiger 4 to chaetigers 8–9. Lateral melanophores on chaetigers 2–6.

Prostomium anteriorly wide, rounded, posteriorly extending to middle of chaetiger 1 as a low narrow caruncle. Occipital antenna not yet developed. Three pairs of black eyes present; lateral eyes situated close to one another and appearing as one pair. One pair of small indistinct unpigmented ocelli situated in front of lateral eyes. Nuchal organs oval ciliary patches posterior to eyes, on sides of caruncle on anterior part of chaetiger 1. Palps arising from postero-lateral edges of peristomium, posterior to prototroch, directed posteriorly and extending to chaetigers 7–8; longitudinal groove lined with numerous short motile cilia present on frontal surface.

Long larval serrated bristles in all notopodia, those of chaetiger 1 longest, as long as 7–8 chaetigers; bristles absent in neuropodia. Short adult capillaries in notopodia from chaetiger 2 onwards, and in neuropodia of chaetigers 1–7. Bidentate hooded hooks in neuropodia from chaetiger 8 onwards, not accompanied by capillaries. Chaetiger 5 as same as chaetiger 4 or 6; three pennoned spines and three falcate spines present among larval bristles in each notopodium.

Proto- and telotroch well developed. Nototrochs and dorso-lateral grasping cilia from chaetiger 3 onwards. Neurotroch narrow, triangular, extending posteriorly over peristomial lip to end of chaetiger 1. Two pairs of small companion ciliated cells present on peristomial lip on sides of neurotroch. Ventral ciliated pit absent. Gastrotrochs on chaetigers 3, 5, 7, 12 and 16. Gastrotroch on chaetigers 3 composed of one pair of small oval cells situated close to midline and oriented almost parallel to body axis; that on chaetiger 5 of four pairs of large transversally elongated cells with long cilia; on chaetiger 7 of three pairs of large transverse cells with long cilia; and on chaetigers 12 and 16 of two pairs of large transverse cells with long cilia.

Branchiae short buds on chaetigers 7 and 8. Pygidium small, with middorsal incision.

Glandular pouches in neuropodia from chaetiger 1, largest and double in each neuropodium in chaetigers 6 and 7, single in other neuropodia.

Large lateral lips of peristomium lined with numerous short cilia, sparsely scattered long compound motile cirri and forming voluminous vestibulum. Ventral peristomial lip triangular, extending over first chaetiger. Digestive tract transparent, without particular pigment. Narrow esophagus extending to end of chaetiger 4. Numerous lipid globules, each up to 10 µm in diameter, present in wall of voluminous midgut. Ventral buccal bulb and gizzard-like structure absent. Circulatory system fully developed and functional; wall of main dorsal blood vessel contracting, pumping blood in anterior direction. Blood without colored pigment. Two pairs of protonephridia in chaetigers 1 and 2. Adult nephridia from chaetiger 4 onwards.

Remarks. Pseudopolydora achaeta was originally described from the mouth of Tsengwen River (South China Sea, Taiwan; Fig. 5 ) as a common polychaete inhabiting tubes in soft sediments ( Radashevsky & Hsieh 2000b). Since then, this species has been reported from Paraná and São Paulo ( Brazil) ( Lana et al. 2006), Peter the Great Bay (Sea of Japan, Russia) ( Moshchenko & Belan 2010; Zvyagintsev et al. 2011), Florida ( USA) ( Bogantes et al. 2021), and the Arabian Gulf ( Kuwait) ( Radashevsky et al. 2021a). Here, for the first time, based on molecular data (see above), we report it for the Caribbean Sea (Martinique) and Nha Trang Bay ( Vietnam). Based on the morphology, we also report this species for the first time for the East Sea ( South Korea) and provide new records for the north-western part of the Sea of Japan ( Russia). Some details of the reproductive biology and larval morphology of P. achaeta are described here for the first time.

Abe et al. (2014, 2016, 2019) and Abe & Sato-Okoshi (2021) reported P. achaeta and P. aff. achaeta from the Pacific side of Honshu ( Japan). However, a comparison of the sequences provided by these authors with sequences of P. achaeta from Taiwan obtained by Radashevsky et al. (2020a) showed that they are not conspecific ( Fig. 1 ). Larvae of P. aff. achaeta from Honshu, briefly described and illustrated by Abe & Sato-Okoshi (2021: fig. 9A, B), are similar to larvae of P. achaeta from Taiwan and Vietnam in general outline, arrangement of gastrotrochs, presence of small paired melanophores on the dorsal side of chaetigers, and a middorsal row of characteristic vesiculate melanophores. However, they differ in the arrangement of these melanophores, beginning from different chaetigers in Japanese and Taiwanese/Vietnamese larvae.

Adult P. achaeta are unique among congeners in their specific pigmentation pattern, arrangement of the notopodial spines of chaetiger 5 in an almost straight vertical row instead of J- or U-shaped rows, and relatively well-developed lateral peristomial lips. These lips are well developed in the larvae of all spionids, but are usually reduced, retracted, and transformed into narrow lateral folds of the foregut during settlement and metamorphosis. The ventral peristomial lip of the larvae, on the contrary, enlarges during metamorphosis and forms the entire peristomium in adults of most spionids. In P. achaeta , the large lateral lips of the larvae are only partially reduced during metamorphosis; therefore, in adults of this species, they make up a great part of the peristomium (see Radashevsky and Hsieh 2000b: fig. 4B, C). Similar body pigmentation and the shape of the peristomium are also present in the adults of Pseudopolydora glandulosa Blake & Kudenov, 1978 from Australia. The relationship between these two species should be explored in a future study.

Distribution. Complete information on earlier and new records of P. achaeta is given in Supplementary Table S1 (mapped in Fig. 5 ).

Figures

FIGURE 1. Majority rule consensus tree of the Bayesian inference analysis of the combined COI (604 bp), 16S (258 bp), 18S (1652 bp), 28S (293 bp), and Histone 3 (307 bp) sequences (3114 bp in total) of Pseudopolydora spp. rooted with sequences of Pseudopolydora dayi Simon, 2009. Posterior probabilities are shown on the branches. The numbers preceding collecting locations are unique numbers from the VIR database linking the individuals on the tree with the sampling data in Table 1 and Supplement Tables S1–S4; numbers of individuals are separated from sample numbers by dots. Colored labels showing not apomorphies but merely characters shared by members of the corresponding clades.

FIGURE 2. Pseudopolydora achaeta adult morphology. A, B, anterior ends, dorsal view. C, D, anterior end, left lateral view. Scale bars: A, B, D = 200 µm; C = 500 µm. A, Nha Trang Bay, Vietnam (MIMB 40946). B, Paranaguá Bay, Paraná, Brazil (MIMB 40945). C, D—Florida, USA (VIR 24579, photos by Michael Scott Jones).

FIGURE 3. Adult morphology of Pseudopolydora achaeta. A, chaetigers 3–6, left lateral view. B, posterior-row falcate spines from notopodium of chaetiger 5. C, hooded hooks from neuropodium of chaetiger 8. Abbreviations: ch3, ch4—chaetigers 3 and 4. Scale bars: A = 30 µm; B = 5 µm; C = 10 µm. A–C—Peter the Great Bay, Sea of Japan, Russia (SEM, VIR 700).

FIGURE 4. Pseudopolydora achaeta larval morphology. A–D, 20-chaetiger larva from plankton: A, dorsal view, in transmitted light; B, same, ventral view; C, dorsal view, in reflected light; D, same, ventral view. Scale bars: A–D = 100 µm. Nha Trang Bay, Vietnam (in life, VIR 25357).

FIGURE 5. Map showing records of Pseudopolydora achaeta (see Table S1). Red star—type locality: Tsengwen River estuary, Tainan Co., Taiwan; green triangles—specimens sequenced in the present and earlier studies; yellow circles—adults identified based on the morphology only.

FIGURE 6. Adult characteristics of Pseudopolydora spp. Relationships between caruncle length (in chaetiger numbers) and total number of chaetigers, and between distribution of branchiae (referring to number of the last branchiate chaetiger) and total number of chaetigers in P. achaeta (A) and P. rosebelae (C). Relationships between distribution of gametes (referring to number of the first and the last chaetigers with gametes) and total number of chaetigers in P. achaeta (B) and P. rosebelae (D). Correlation coefficients (r) and equations (y) for the distribution of branchiae and the total number of chaetigers are presented in the corresponding graphs. All correlations are significant (P <0.05).