Manayunkia aestuarina ( Bourne, 1883 )

Bick, Andreas & Bastrop, Ralf, 2025, Revision of the genus Manayunkia Leidy, 1859, and establishment of two subfamilies within Fabriciidae (Annelida, Sabellida), Zootaxa 5661 (1), pp. 1-58 : 12-16

Manayunkia aestuarina ( Bourne, 1883)

( Figures 3 top left, 5–8, 26A)

Haplobranchus aestuarina Bourne, 1883: p. 168 –176, pl. 9, fig. 1–14.

Haplobranchus balticus Karling, 1933: p. 242 –244, fig. 1.

Manayunkia aestuarina . – Zenkevitsch, 1925: p. 38 –39. – Bishop 1984: 389–390.

? Manayunkia polaris Zenkevitsch, 1935: p. 195 –202.

Not Manayunkia aestuarina . – Harris 1970: 106–107, fig. 1.

Material examined. Baltic Sea: 54°01’60.00’’N, 11°29’59.99’’E, depth 0.5 m, coll. 06.06.1996,> 100 specimens ( ZSRO-P1005 ) , 54.02581N, 11.531032E, depth 0.5 m, coll. 22.04.1997,> 100 specimens ( ZSRO-P1008 ) ; 54°01’26.2’’N, 11°29’23.9’’E, depth 0.5 m, coll. 26.04.1982,> 100 specimens ( ZSRO-P1076 ) .

Description. Total length of specimens, including radiolar crown, between 2.5 and 6 mm; width on chaetiger two about 0.2 mm; length of radiolar crown about 0.25–0.35 mm; ratio between length of radiolar crown and body length, without radiolar crown, between 0.1 and 0.15. Body slender, slightly tapering posteriorly ( Figs 3 , 5A, K ).

Radiolar crown with three pairs of radioles and one pair of unbranched vascularized ventral filamentous appendages, surface of radioles and ventral filamentous appendages wrinkled ( Figs 5B, C , 6A , 26A ); dorsal and median radioles unbranched, ventral radioles with two branches ( Figs 6B–F , 26A ); no morphological differences in the structure of the branches of the radiolar crown, except ventral filamentous appendages ( Figs 5C , 6B ); ventral filamentous appendages and branches of the radioles end at about same height or ventral filamentous appendages slightly longer ( Fig. 5A–C ); radioles and vascularized ventral filamentous appendages rectangular, square or rounded in cross-section; extension about 25–40 x 30–45 µm and 45–60 x 55–70 µm, respectively ( Fig. 6B ); ventral filamentous appendages with clearly visible blood vessel ( Fig. 6B–F ).

Epidermis of all branches of radioles and vascularized ventral filamentous appendages with ciliated and non-ciliated epithelial cells; epithelial cells of branches of radioles with microvilli and a 1–2 µm thick cuticle ( Fig. 7A, B ); 9–10 epithelial cells with 3–12 cilia each constitute the shallow or even convex food groove of radioles adorally; most laterally located epithelial cells of food groove, each with 6–7 significantly longer laterofrontal cilia ( Fig. 7A, B ); occasionally 2–3 aboral cilia present ( Fig. 7B, F ); number of epithelial cells of radioles decreases from base to tip; cilia completely absent at the tip, microvilli and cuticle present ( Fig. 7E ); epithelial cells with many mitochondria, intracellular glycogen and vacuoles; glycogen and vacuoles located almost exclusively basiepithelial ( Fig. 7A ); aboral epithelial cells with longitudinal myofibrils forming a longitudinal muscles of branches of radioles; 1–3 intraepithelial nerves aborally, up to 3 intraepithelial nerves adorally; center of branches of radioles occupied by large coelomic cavity bordered by flat myoepithelial cells, about 1 µm wide ( Fig. 7A, B, D ); between epidermal and myoepithelial cells an extracellular matrix, about 0.2 µm wide; extracellular matrix with irregularly arranged collagen fibres ( Fig. 7A–F ); narrow cytoplasmic processes with a length of about 1-3 µm extend into coelomic cavity of branches of radioles ( Fig. 7D, F ); dorsal lips developed as rounded lobes with a length of about 40 to 50 µm ( Fig. 6E, F ).

Peristomium slightly longer than first chaetiger, about as long as chaetiger 2, with anterior and posterior rings; anterior peristomial ring distinctly shorter than posterior ring ( Fig. 5A–C ); anterior margin developed as a low membranous collar ventrally, narrowly separated mid-dorsally ( Figs 5B, C , 6A ); ciliated band on posterior margin of anterior peristomial ring ventrally ( Figs 5C , 6A ); border between anterior and posterior peristomial rings clearly visible all around ( Figs 5B, C , 6A ); one pair of rounded black peristomial eyes present ( Fig 3 ); females with pigmented spermathecae.

Metanephridia in peristomium and chaetigers 1 and 2. First thoracic chaetiger shorter than peristomium and second chaetiger; chaetigers 2–6 successively longer; chaetiger 8 shorter than chaetiger 7; first 3 or 4 thoracic chaetigers wider than long, chaetigers 4 or 5–8 distinctly longer than wide; abdomen about as long as chaetiger 7; first abdominal chaetiger longest, about twice as long as second one; abdominal chaetiger 3 slightly shorter than second, about as long as pygidium; Pygidium tapered or terminating as rounded lobe ( Figs 3 , 5A, K ); pygidial eyes absent; borders between thoracic and abdominal chaetigers usually clearly visible ( Figs 3 , 5A, K ).

First chaetiger with about 1–2 short, and 2–3 elongate, narrowly hooded notochaetae, neuropodial uncini absent; notopodia of chaetigers 2–8 superiorly with 3–6 elongate, narrowly hooded chaetae, inferiorly with 1–2 (rarely 3) pseudo-spatulate chaetae on chaetigers 2–5 and 1–3 short, narrowly hooded chaetae on chaetigers 6–8 ( Fig. 5E, F ); neuropodia of chaetigers 2–8 (male) or 2–5 (female) with 5–8 uncini with main fang and apical with about 4–5 rows of progressively smaller teeth ( Fig. 5G ); females with 5–12 transitional uncini on chaetigers 6–8, different from thoracic uncini on chaetigers 2–5; transitional uncini longer than regular thoracic uncini, without main fang, with a multitude of rows of small, equal-sized teeth ( Fig. 5H ); abdominal neuropodia with 2–5 elongate and 1–2 short, narrowly hooded chaetae ( Fig. 5D ); abdominal notopodia with 15–22 uncini on chaetiger 9, 12–15 uncini on chaetiger 10, and 8–12 uncini on chaetiger 11, respectively; abdominal uncini with about 6–7 rows of equal-sized teeth, about 4–6 teeth per row ( Fig. 5I ); manubrium about 3 times as long as dentate region.

Females with shallow brood chamber on chaetigers 6 and 7 or 8, formed by wing-like protrusions of the integument of these chaetigers; brood chamber segments not elongated and chaetiger boundaries clearly visible.

Fixed specimens usually translucent, however radiolar crown, anterior intestinal region and nephridia brownish in colour; ventral vascularised filamentous appendages of living animals greenish, due to colour of blood ( Fig. 26A ).

Remarks. Manayunkia aestuarina is the species of the genus with the largest area of distribution. Based on genetic studies, this species has at least a transatlantic distribution ( Huang et al. 2011). However, whether the occurrence of Manayunkia specimens on the Pacific coast ( Bishop 1984; Light 1969) and the Iberian Peninsula ( López & Cepeda 2017) can actually be attributed to this species, or whether they are misidentifications, remains to be clarified. The individuals described as M. aestuarina by Harris (1970) from marine habitats of the Isles of Scilly, Great Britain, certainly do not belong to this species. These individuals lack pseudo-spatulate chaetae and the radiolar crown is also very different from that characteristic of M. aestuarina . The synonymisation of M. polaris with M. aestuarina assumed by Zenkevitsch (1935) and Hartman (1951) should also be critically reviewed.

Manayunkia aestuarina is the species with the lowest number of branches of the radioles. At an early stage of larval development, the structure of the radiolar crown is already clearly recognizable. There are 3 radioles that originate from a common base. Only the ventral radiole divides into 2 branches, the other two remain unbranched ( Fig. 8A, B ). All other Manayunkia species have more than 4 pairs of branches (see Table 2).

In the literature, lengths of up to 4–6 mm (probably living individuals) are given for this species (e.g., Bourne 1883; Hartmann-Schröder 1996; Karling 1933; Zenkevitsch 1925). In the Baltic Sea, fixed specimens usually reach 2 mm, only some preserved specimens are slightly larger.

The TEM examinations showed that the ECM as a possible radiolar skeleton is only very weakly developed. In Fabriciinae subfam. nov., on the other hand, the ECM is strongly developed adorally and can be described as a true supporting structure ( Fig. 4E ). The number of cells forming the feeding groove also differs from those found in various Fabriciinae species ( Randel & Bick 2012; Bick 2020; Tilic et al. 2021).

This species is sexually dimorphic. In females, transitional uncini were found in chaetigers 6–8. In some other Manayunkia species, such transitional uncini or transitional chaetae have also been found in females (see Remarks for other species). The occurrence of transitional uncini in this species is described here for the first time. As these uncini differ very little from the regular thoracic uncini, it is difficult to observe them under the light microscope. This could explain why this type of uncini has not yet been described. The presence of a brood chamber in females is also described here for the first time.

The number of thoracic and abdominal uncini increases with total length of specimens. Small specimens have hardly more than 20 uncini per body side in the three abdominal chaetigers, whereas adults have more than 50 ( Bick 1995).

Geographic distribution. This species is found in brackish waters of the North Atlantic, both on European and American coasts, and probably also on the Pacific coast of North America.

Biology. Abundances of more than one million specimens per square meter have been reported for M. aestuarina in suitable habitats (e.g., Bagheri & McLusky 1982; Bell 1982). Spermiogenesis occurs in chaetigers 6 to 8, and egg development in chaetiger 4. According to Forsman (1956) and Schütz (1965), M. aestuarina females are 3–5 times as numerous as males, but Bick (1996) found a sex ratio of approximately 1: 1 in the southern Baltic Sea. Manayunkia aestuarina females exhibit between two and four eggs. The reproduction of M. aestuarina is discontinuous, as neither embryos nor juvenile recruitment was observed during winter months (November to March) in a South Carolina salt marsh ( Bell 1982). Reproduction also starts at the end of March/beginning of April in the southern Baltic Sea but is completed by the end of August, as no eggs or larvae are found in the female tubes after August ( Bick 1996; Schütz 1965). Males reach reproductive maturity before females in the Baltic Sea ( Bick 1996). Males with sperm and females with eggs have been observed in autumn and winter in the North Sea ( Schütz 1965). On average, 4 eggs of approximately 200–300 µm in length and developing larvae are simultaneously found within a tube, with a maximum number of 16 occurring in the middle of the reproductive period. Bell (1982) observed 8– 12 larvae per tube, each of which was in a different stage of development. The youngest stages generally occupied the anterior part of the tube, with the more advanced larvae behind them. All larvae faced the tube mouth, and all stages were joined by a mucous coating. The development of larvae may take two weeks ( Forsman 1956), from two to four weeks ( Bell 1982) or eight weeks ( Bick 1996). Low temperatures delay the development time. The larvae leave the tube at a size of about 0.6–0.7 mm ( Bick 1996). They do not crawl far from the female tube. The survival rate of juveniles is approximately 15–20%, and the average age of this species is approximately one year ( Bick 1996).

High temperatures, lack of oxygen or other unfavourable parameters cause M. aestuarina to extend the posterior end out of the tube and perform circular movements. Not infrequently, the radiolar crown is then thrown off ( Schütz 1965). Outside of the tubes, the worm encases itself in mucus and shows great chaetal activity in the search for a suitable substratum ( Knight-Jones 1981).

Manayunkia aestuarina has a range of feeding mechanisms, but is thought to be mainly a deposit feeder ( Lewis 1968).

Ecology. Manayunkia aestuarina lives preferably in tubes in muddy to fine sand in shallow brackish water areas. The presence of peritrich ciliates as commensals was described for M. aestuarina from the Baltic Sea ( Bick 2020). These were located on the first thoracic chaetigers in close proximity to the notopodia.

Figures

FIGURE 3. Drawings of M. aestuarina (Bourne, 1883) on the left and M. athalassia Hutchings, Decker & Geddes, 1981 on the right, including chaetae and uncini types found in Manayunkia species.

FIGURE 4. Fabriciinae subfam. nov.; A–E Fabricia stellaris (Müller, 1774) from the Baltic Sea. A. Total view of a living individual. B. Radiolar crown of a living specimen. C. SEM micrograph of radiolar crown, dorsal view. D. Anterior end, ventral view (arrow points to ciliated patch of the anterior peristomial ring lobe). E. TEM micrograph of a branch of a radiole. Scale bars. A–B 200 µm, C 100 µm, D 50 µm, E 3 µm µm (abbr: bh branchial hearts, ecm extracellular matrix, pre peristomial eyes, pye pygidial eyes, sp spermatheca).

FIGURE 5. Manayunkia aestuarina (Bourne, 1883), SEM micrographs. A. Total view of complete specimen, ventral view. B. Anterior end, dorsal view. C. Anterior end, ventral view. D.Abdominal neurochaetae of chaetiger 9. E. Notopodium of chaetiger 5, with pseudo-spatulate chaetae inferiorly. F. Notopodium of chaetiger 8, with short, narrowly hooded chaetae inferiorly. G. Thoracic uncini of chaetiger 2. H. Parapodium of chaetiger 6 with 5 transitional uncini. I. Abdominal uncini of chaetiger 9. K. Posterior end, lateral view. Scale bars. A 500 µm, B, C, K 100 µm, D–F, H, I 10 µm, G 5 µm.

FIGURE 6. Manayunkia aestuarina (Bourne, 1883), semithin sections (1 µm) of the radiolar crown.A. SEM micrograph of the base of the radiolar crown with the estimated position of the section level in figures B–F. B. Branches of three pairs of radioles and one pair of ventral vascularized filamentous appendage, all separated. C. Branches of right ventral and median radioles start to fuse with one another (35 µm basal of section B). D. Right ventral and median radioles fused, all other radioles separated (15 µm basal of section C). E. Right ventral, median and dorsal radioles fused, dorsal lips visible (10 µm basal of section D). F. Right dorsal lip fused with ventral vascularized filamentous appendage, and left dorsal lip fused with left dorsal radiole; branches of left ventral radiole fused (30 µm basal of section E). Scale bars. B–F 50 µm (abbr: dl dorsal lips, dr dorsal radiole, mr median radiole, vvfa ventral vascularized filamentous appendages, vr ventral radiole).

FIGURE 7. Manayunkia aestuarina (Bourne, 1883), TEM micrographs.A. B Cross-section of a branch of a radiole at the base. C. Extracellular matrix between both epithelia. D. Cross-section of a branch of a radioles near the tip. E. Cross-section of a branch of a radiole at the tip. F. Aboral section of a branch of a radiole. Scale bars. A, B 10 µm, C 0.2 µm, D 5 µm, E 2 µm, F 1 µm. (ab aboral, ad adoral, adc adoral cilia, c coelom, cp cytoplasmic projections, cu cuticle, ecm extracellular matrix, fc, frontal cilia of the food groove, gly glycogen, lfc latero-frontal cilia of the food groove, m mitochondria, mv microvilli, myo myoepithel cell, n nucleus, vac vacuole).

FIGURE 8. Manayunkia aestuarina (Bourne, 1883), SEM micrographs. A. Radiolar crown of larva, ventro-lateral view. B. Radiolar crown of a larva, dorso-lateral view. (Note the common base of the three radioles and the division of ventral radioles in to 2 branches each in Fig. A and Fig. B). Scale bars. A, B 200 µm.

FIGURE 26. Live images of the radiolar crown of two Manayunkia species. A. Radiolar crown of M. aestuarina (Bourne, 1883), with one branch of dorsal radioles, one branch of median radioles and two branches of ventral radioles. B. Radiolar crown of M. athalassia Hutchings, Decker & Geddes, 1981, with four branches of dorsal radioles, five branches each of median radioles and ventral radioles. (abbr: vvfa unbranched ventral vascularized filamentous appendages).