Pseudopolydora rosebelae Radashevsky & Migotto, 2009

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 : 223-229

Pseudopolydora rosebelae Radashevsky & Migotto, 2009

Figures 6C, D , 7–11

Pseudopolydora rosebelae Radashevsky & Migotto, 2009: 462–467 , figs 1–6. Bogantes et al. 2021: 584, fig. 3A, B. Pseudopolydora sp. A : Radashevsky & Migotto 2006: fig. 2a.

Not Pseudopolydora cf. rosebelae : Radashevsky 2015: 682–684 , figs 31, 32.

Type material examined. Brazil, São Paulo: São Sebastião Is. (Ilhabela), Praia do Sino , 23.74696ºS, 45.34844ºW, 5 m, sandy silt, coll. Radashevsky V.I., 15 April 2004, MZUSP 243 (holotype); MIMB 27220 (1 paratype); MZUSP 241 , 242 (2 paratypes); SMF 16856 (2 paratypes); ZUEC POL 20 (2 paratypes) .

Other material examined. Belize: USNM 1480640 (1).

Brazil, Rio de Janeiro: MNRJ 067 (1).

Thailand, Gulf of Thailand: LACM-AHF Poly 4395 (3).

USA, Hawaii: MIMB 42734 (1), 42735 (1).

Vietnam, Nha Trang Bay: MIMB 27221 (5), 42736–42738 (4); VIR 13862 (1).

Full information about the samples is given in the Supplementary Table S2.

Adult diagnostic characters. Adults up to 20 mm long, 1.1 mm wide for 55 chaetigers ( Figs 7A , 8A, B , 9A ). Body transparent, light yellowish in life, with intense black pigment and small white stellar chromatophores on prostomium, peristomium, and dorsal side of 5–7 anterior chaetigers ( Figs 7A–E , 8A–D , 9A–C ). Palps in large individuals with up to 22 black transverse bands ( Fig. 10A, C ). Prostomium anteriorly bilobed, extending posteriorly to end of chaetiger 1 as a low caruncle ( Fig. 6C ). Occipital antenna present. Two to three pairs of black eyes present. Thin epithelial hood arising from dorsal anterior edge of chaetiger 3 and forming voluminous pouch over chaetiger 2 ( Figs 7C, D , 9B ). Chaetiger 1 weakly separated from peristomium, without notochaetae, with short capillaries in neuropodia; small lamellae present in both rami. Chaetigers 2–4 and 6 with slender capillaries in both rami. Chaetiger 5 similar in size to chaetigers 4 or 6, with short postchaetal lamellae in neuropodia; notopodial lamellae reduced; dorsal superior capillaries slightly shorter and fewer than those chaetae on chaetigers 4 or 6; 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 J-shaped double row ( Figs 7E , 9B , 10C ): anterior-row spines pennoned, with curved pointed tip, up to ten in a series; posterior-row spines simple falcate, up to eight in a series. Posterior notopodia with only slender capillaries. Bidentate hooded hooks in neuropodia from chaetiger 8, up to 10 in a series. Branchiae from chaetiger 7, up to 18 pairs ( Fig. 6C ). Pygidium large cup with middorsal gap ( Figs 7A , 8E , 10B ). 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. Blood transparent, without colored respiratory pigment. Nephridia from chaetiger 4 onwards.

Habitat. Adults of P. rosebelae live in silty tubes in muddy sand in shallow water. The tubes are up to 50 mm long, 2 mm wide, and protruded above the sediment up to 5 mm. The species is rare. The population density is usually several individuals per 1 m 2.

Reproduction. Pseudopolydora rosebelae is probably parthenogenic. All 14 mature individuals studied (10 from Brazil and 4 from Vietnam) were females. The worms become mature after they have grown to about 10 mm long with 40 chaetigers. Oocytes develop from chaetigers 14–15 to chaetigers 24–36 ( Figs 6D , 7A, F , 8A–D , 9A ). Paired ovaries are attached to segmental blood vessels in fertile chaetigers. Mature oocytes are about 150 µm in diameter. Females lay up to 400 oocytes in 23 capsules joined in a string and each attached by one stalk to the inside wall of the tube. The larvae develop inside the capsules until 4-chaetiger stage, and then they hatch and continue their development in sea water. They settle and metamorphose after growing to 1.2–1.5 mm long with 15–18 chaetigers ( Radashevsky & Migotto 2009).

Larval morphology. Larval development of P. rosebelae from Brazil was described by Radashevsky & Migotto (2009). Pelagic larvae of this species are easily recognized by their characteristic pigmentation: three pairs of yellow subspherical chromatophores in the prostomium and peristomium, numerous chromatophores on the dorsal and ventral sides of chaetigers, and large ramified mid-dorsal melanophores on chaetiger 1 and from chaetiger 3 onwards. Larvae described and illustrated below were collected from Nha Trang Bay ( Vietnam) in May 2022. They appeared similar to larvae from Brazil.

The 13-chaetiger larvae are about 900 µm long ( Fig. 11A–F ). Yellow pigment diffused on anterior part of prostomium, dorso-lateral sides of peristomium, on pygidium and on some chaetigers. Three pairs of large yellow subspherical chromatophores inside lateral peristomial lips, close to their ventral side; smaller yellow chromatophores on dorsal and lateral sides of chaetiger 1, and on dorso-lateral sides from chaetiger 5 to chaetigers 10–11 above melanophores; large midventral chromatophores usually on chaetigers 5, 7 and 12; single or one pair of chromatophores on ventral side of pygidium. Chromatophores changing their shape from compact to greatly ramified according to light intensity or condition of larvae. Single middorsal melanophore on chaetiger 1 usually large, ramified, occasionally reduced or even absent. Large ramified middorsal melanophores from chaetiger 3 onwards; melanophore on chaetiger 3 largest, extending onto posterior part of chaetiger 2; melanophore on chaetiger4 slightly smaller, extending onto posterior part of chaetiger 3; melanophore small on chaetigers 6–8, and large and greatly ramified on succeeding chaetigers. One pair of small ramified melanophores in posterior edges of ventral peristomial lips. One pair of small lateral melanophores on anterior edges of chaetiger 2. Dorso-lateral ramified melanophores from chaetiger 4 to chaetigers 8–9.

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, comprising one pair of simple cup-shaped median eyes, one pair of double lateral eyes, and one pair of cup-shaped eyes between median and lateral eyes ( Fig. 11F ). One pair of small indistinct unpigmented ocelli situated in front of pigmented eyes. Nuchal organs oval ciliary patches posterior to eyes, on sides of caruncle, partly at level of prototroch and partly on anterior part of chaetiger 1 ( Fig. 11F ). Palps smooth, without ciliation, arising from postero-lateral edges of peristomium, posterior to prototroch, directed posteriorly and extending slightly beyond first chaetiger.

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; short single pennoned spine present among larval bristles in notopodia.

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 and 12. Gastrotroch on chaetigers 3 composed of one pair of small oval cells situated close to midline; that on chaetiger 5 of four pairs of large transversally elongated cells with long cilia; on chaetiger 7 of six pairs of large transverse cells with long cilia; and on chaetiger 12 of four pairs of small cells with short cilia.

Branchiae not yet developed. Pygidium small, with middorsal incision.

Glandular pouches in neuropodia of chaetigers 6–11, 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 ( Fig. 11E ). Ventral peristomial lip triangular, extending over first chaetiger. Digestive tract transparent, without particular pigment. Narrow esophagus extending to end of chaetiger 3. Numerous lipid globules, each up to 20 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 in chaetigers 4–10.

The 14-chaetiger larvae are about 950 µm long ( Fig. 11G–I ). They appear similar to previous stage but differ by the presence of slightly longer palps with shallow frontal groove lined with fine cilia, 3–4 pennoned spines and 1–2 simple falcate spines in each notopodium of chaetiger 5, and three pairs of short branchiae on chaetigers 7–9.

Remarks. Pseudopolydora rosebelae was originally described from the states of São Paulo and Rio de Janeiro ( Brazil) by Radashevsky & Migotto (2009) ( Fig. 12 ). Since then, outside of Brazil, this species has only been reported from Florida ( Bogantes et al. 2021). Adults are unique among spionids for their pigmentation pattern (intense black and white pigment on the dorsal side of the head and anterior chaetigers), dorsal hood over the second chaetiger, and transparent blood without colored respiratory pigment. This species is rare, and all mature worms examined to date were females. Very few individuals have been found in Belize, Brazil, Thailand, Florida and Hawaii, and here we report for the first time 11 individuals from Vietnam despite intensive collections in this region (see Britayev & Pavlov 2007, 2012, 2013). Molecular data on this species has not been available to date. Genetic comparison of specimens from Brazil and Vietnam performed in this study showed that they are conspecific ( Fig. 1 ; Table S6).

An anterior fragment of a small worm similar to P. rosebelae was found off Lizard Island (Queensland, Australia) by Radashevsky (2015). The fragment differed from the Brazilian spcimens in the absence of black pigment on the anterior chaetigers and was therefore tentatively identifed as P. cf. rosebelae . Genetic comparison of specimens from Brazil and and Vietnam with the single specimen from Australia performed in this study showed that they are not conspecific ( Fig. 1 ; Table S6). The Australian specimen is described below as a new species, P. nivea sp. nov.

Of the 12 examined individuals from Brazil (up to 20 mm long, with 45–55 chaetigers), six worms were with palps, of which two individuals (with 48 and 50 chaetigers) had only yellowish pigment along the frontal ciliated groove, and four individuals separately had 6, 7, 21 (holotype) and 22 small black transverse bands regularly arranged along each palp ( Radashevsky & Migotto 2009: fig. 2B). Most examined worms from Vietnam were small, up to 10 mm long, with 45 chaetigers, and had only dark yellowish pigment on palps ( Fig. 8A, B ); one 55-chaetiger individual had characteristic black transverse bands on palps ( Fig. 10C ).

Distribution. Complete information on earlier and new records of P. rosebelae is given in Table S2 (mapped in Fig. 12 ).

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 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).

FIGURE 7. Pseudopolydora rosebelae adult morphology. A, 51-chaetiger female, left lateral view, palps missing. B, same, anterior end, dorsal view. C, anterior end, left lateral view. D, anterior end, dorsal view, palps missing. E, same, left lateral view. F, same as A, middle fertile segments, left lateral view. Abbreviations: ch5—chaetiger 5; gl—glandular pouches in neuropodia of chaetigers 6 and 7; ho—epithelial hood arising from dorsal anterior edge of chaetiger 3 and forming a prominent pouch above chaetiger 2; ne—nephridia in female fertile chaetigers. A, B, D–F—in reflected light; C—in transmitted light. Scale bars: A = 1 mm; B–F = 300 µm. A, B, F—São Paulo, Brazil (in life, paratype ZUEC-POL 20, photos by Álvaro Migotto). C—Nha Trang Bay, Vietnam (in life, MIMB 42737). D, E—Fort Pierce, Florida, USA (formalin-fixed, VIR 24373, photos by Michael Scott Jones).

FIGURE 8. Pseudopolydora rosebelae adult morphology. A, 45-chaetiger female, dorsal view, right palp broken. B, same, left lateral view. C, anterior end, dorsal view. D, same, ventral view. E, posterior end, dorsal view. Scale bars: A, B = 1 mm; C, D = 300 µm; E = 10 µm. A–E—Nha Trang Bay, Vietnam (in life, MIMB 42737, photos by Sergey Garin).

FIGURE 9. Pseudopolydora rosebelae adult morphology. A, 45-chaetiger female, left lateral view, palps missing. B, same, anterior end, left lateral view. C, same, dorsal view. Abbreviations: an—occipital antenna; ho—epithelial hood arising from dorsal anterior edge of chaetiger 3 and forming a prominent pouch above chaetiger 2. Scale bars: A–C = 200 µm. A–C—Nha Trang Bay, Vietnam (in life, MIMB 42738).

FIGURE 10. Pseudopolydora rosebelae adult morphology. A, anterior end, ventral view. B, posterior end, dorsal view. C, anterior end, left lateral view. Scale bars: A–C = 200 µm. A—Hawaii (formalin-fixed, MIMB 42734); B—Hawaii (formalinfixed, MIMB 42735); C—Nha Trang Bay, Vietnam (formalin-fixed, MIMB 42736).

FIGURE 11. Pseudopolydora rosebelae larval morphology. A–F, 13-chaetiger larva from plankton: A, dorsal view, in transmitted light; B, same, ventral view; C, dorsal view, in reflected light; D, same, ventral view; E, anterior end, ventral view; F, head, dorsal view. G–I, 14-chaetiger larva from plankton: G, dorsal view, in transmitted light; H, same, in reflected light; D, same, ventral view. Abbreviations: la—lateral peristomial lip; pa—palp; ve—ventral peristomial lip. Scale bars: A–I = 100 µm. A–I—Nha Trang Bay, Vietnam (in life, MIMB 42738).

FIGURE 12. Map showing records of Pseudopolydora spp. Pseudopolydora rosebelae: red star—type locality:São Sebastião Is. (Ilhabela), São Paulo, Brazil; green triangles—specimens sequenced in the present study; yellow circles—adults identified based on the morphology only (see Table S2). Pseudopolydora nivea sp. nov.: turquoise star—type locality: Lizard Is., Queensland, Australia; holotype sequenced in the present study (see Table S4).