Manayunkia caspica Annenkova, 1929

Bick, Andreas, Oberrisser, Philipp & Bastrop, Ralf, 2024, Redescription of Manayunkia caspica Annenkova, 1929 and M. danubialis Băcescu, 1944 n. comb. (Fabriciidae, Sabellida, Polychaeta), Zootaxa 5477 (4), pp. 445-464 : 449-455

Manayunkia caspica Annenkova, 1929

( Figures 2–5 )

Manayunkia caspica Annenkova, 1929a: 18–20 , pl. 3, fig. 1–4, pl. 4, fig. 10–12. Zenkewitsch.—1935: 198–201.— Hartman 1951: 389.

Diagnosis. Eight thoracic and three abdominal chaetigers. Pectinated radioles present. Unbranched vascularized ventral filamentous appendages present. Dorsal lips erect, rounded. Anterior margin of anterior peristomial ring developed as a low membranous collar with distinct ventral lobe; anterior peristomial ring narrowly separated mid-dorsally; ciliated band ventrally on the posterior margin of the anterior peristomial ring. Border between anterior and posterior peristomial rings clearly visible. Inferior thoracic notochaetae on chaetigers 1 and 6–8 narrowly hooded, and pseudospatulate on chaetigers 2–5. Thoracic uncini of chaetigers 2–5 or 2–8 (sexual dimorphism?) with a main fang and towards apical with about 4–5 rows of progressively smaller teeth. When these uncini are absent (females?), i.e., segments 6–8, transitional uncini present; transitional uncini without main fang and a multitude of rows of small, equal-sized teeth. Dentate region of abdominal uncini with about 5–6 rows of equal-sized teeth, manubrium about three to four times as long as dentate region. Peristomial eyes black, pygidial eyes absent. Females with pigmented spermathecae and brood chamber.

Material examined. Russia, Eurasia , Caspian Sea: 43°57.733’N, 48°37.840’E, depth 28.7 m, date 12.10.2018, 23 specimens ( ZMMU WS 19181 (12 ind.) and ZSRO-P2695 (11 ind.), 43°57.733’N, 48°840’E, depth 28.7 m, date 12.10.2018, 35 specimens ( ZMMU WS 19182 (17 ind.) and ZSRO-P2696 (18 ind.)), 43°57.733’N, 48°18.100’E, depth 25.7 m, date 10.10.2018, 14 specimens ( ZMMU WS 19183 (9 ind.) and ZSRO-P262697 (5 ind.)) .

Description. Specimens with eight thoracic and three abdominal chaetigers ( Fig. 2A ); total length of specimens, including radiolar crown, between 1.8 mm and 4.2 mm; width between 0.15 mm and 0.22 mm; length of radiolar crown between 0.22 mm and 0.40 mm; ratio between length of radiolar crown and body length, without radiolar crown, between 0.1 and 0.2; body cylindrical, slender, slightly tapering posteriorly ( Fig. 2A, I ).

Radiolar crown with three pairs of radioles and one pair of unbranched vascularized ventral filamentous appendages; surface of radioles and ventral filamentous appendages wrinkled ( Fig. 2B, C, E ); first dorsal radioles branch off from the branchial lobe, median and ventral radioles arise from a common base ( Fig. 4A–E ); ventral and median radioles asymmetrical branched or pectinated, dorsal radioles unbranched; ventral radioles with 6 (left lobe) or 5 (right lobe) branches, median radioles with 3 (left) or 2 (right) branches (only one specimen examined) ( Fig. 4A–F ); no morphological differences in the structure of the branches, except ventral filamentous appendages ( Fig. 4A–B ); ventral filamentous appendages and branches of the radioles end at about same height ( Fig. 2A–C, E ); branches of radioles and vascularized ventral filamentous appendages rectangular to square in cross-section, extension about 20–28 x 24–40 µm and 32–40 x 38–56 µm, respectively ( Fig. 4A ); vascularized ventral filamentous appendages with blood vessel ( Fig. 4A–F ), connecting to corresponding dorsally located branchial heart ( Fig. 5A ); epidermis of radioles and vascularized ventral filamentous appendages medially with ciliated and laterally with non-ciliated epithelial cells; ciliated cells constitute a shallow food groove of radioles ( Fig. 4A, B ); center of branches of radioles occupied by a large cavity bordered by a narrow band of cells; radioles with cylindrical cells laterally; extracellular matrix not visible between epithelia ( Fig. 4A, B ). Dorsal lips as triangular lobes, rounded at upper margin, with ciliated epithelium all around ( Fig. 4C–F ); about 30 to 40 µm long; dorsal lips connect dorsal radioli with vascularized ventral filamentous appendages; between base of branchial lobes and base of dorsal lips, ciliated food groove forms as a continuation of the ciliated epithelial cells of the radioles, which extends ventrally to the mouth opening; mouth opening bounded ventrally by the anterior peristomial ring. Ventral lips or lip-like processes absent.

Peristomium slightly longer than first chaetiger, about as long as chaetiger 2, consisting of anterior and posterior ring; anterior peristomial ring distinctly shorter than posterior ring ( Fig. 2A–C, E ); anterior margin developed as a low membranous collar ventrally, narrowly separated mid-dorsally ( Figs 2B, C, E , 4F , 5A, B ); ciliated band present on collar of anterior peristomial ring ( Figs 2B, E , 5A ); border between anterior and posterior peristomial rings clearly visible all around ( Fig. 2B, C, E ); one pair of rounded black peristomial eyes present ( Fig. 5B ). Females with pigmented spermathecae.

Faecal groove dorsally deeply sunken in peristomial region, becoming considerably lower on first and following chaetigers ( Figs 2C , 5A, B ); faecal groove shifts from dorsal to ventral midline at border between thorax and abdomen ( Fig. 2I ).

Metanephridia in peristomium and chaetigers 1 and 2; nephridial duct paired first and then unpaired; nephropore located dorsally between base of radiolar lobes ( Fig. 5A–B ).

First thoracic chaetiger shorter than peristomium and second chaetiger; chaetigers 2–7 successively longer; chaetiger 8 shorter than chaetiger 7 ( Fig. 2A, E ); first 3 thoracic chaetigers wider than long, chaetiger 4–8 distinctly longer than wide ( Fig. 2A ); first abdominal chaetiger long, about twice as long as second one; abdominal chaetiger 3 slightly shorter, about as long as pygidium; pygidium tapered ( Fig. 2A, I ); pygidial eyes absent; borders between anterior thoracic and abdominal chaetigers clearly visible, but difficult or impossible to identify on chaetigers in females with brood chamber, i.e., between chaetigers 6 and 7 ( Fig. 2A, F ).

First chaetiger with about 2–4 short and 3–5 elongate, narrowly hooded notochaetae, neuropodial uncini absent; notopodia of chaetigers 2–5 superiorly with 3–5 (rarely 6) elongate, narrowly hooded and inferiorly with 2–4 pseudospatulate chaetae ( Fig. 3A–C ); notopodia of chaetigers 6–8 superiorly with 3–5 elongate, narrowly hooded and 2–4 short, narrowly hooded chaetae; neuropodia of chaetigers 2–6 or 2–8 with 2–4 (rarely 5) uncini with main fang and towards apical with about 4–6 rows of progressively smaller teeth ( Fig. 3D–F ); some specimens with 3–8 transitional uncini on chaetigers 6–8, different from thoracic uncini on chaetigers 2–5; apical region of transitional uncini longer than those of regular thoracic uncini uncini, without main fang, with a multitude of rows of small, equal-sized teeth ( Fig. 3G, H ); abdominal neuropodia with 2–3 elongate and 1–2 short, narrowly hooded chaetae ( Fig. 3I ); abdominal notopodia with 12–17 uncini on chaetiger 9, 8–15 uncini on chaetiger 10, and 7–12 uncini on chaetiger 11, respectively; uncini with about 6 rows of equal-sized teeth, about 4–6 teeth per row ( Fig. 3K ); manubrium about 2–4 times as long as dentate region.

Females with brood chamber on chaetigers 6 and 7. Fixed specimens usually without colour and translucent, only anterior peristomial ring sometimes slightly pigmented.

The tube consists of mucus and fine sediment particles. It is significantly longer than the worm that inhabits it ( Fig. 2D ).

Remarks. There are relatively few diagnostic characters to distinguish Manayunkia species. These are especially the number of branches of the radioles, the presence or absence of pseudospatulate chaetae on thoracic chaetigers and transitional chaetae or transitional uncini. In all these characters M. caspica most closely resembles the species M. danubialis n. comb. from the river Danube described below. This certainly led to the assignment of the specimens from the Danube to this Caspian Sea species, albeit as a subspecies (see Introduction and below). However, a comparison of the individuals available to us also showed that there are differences between the specimens from the two areas. In M. caspica , for example, the thoracic chaetigers become continuously longer from chaetiger 2 to chaetiger 7, whereas in M. danubialis n. comb. chaetiger 5 is shorter than chaetigers 4 and 6. Manayunkia caspica has 2–5 (rarely 6) thoracic uncini, whereas M. danubialis n. comb. has 6–8 (rarely 4) uncini. In M. danubialis n. comb. the thoracic uncini are sometimes arranged in a slightly offset double row. In addition, the thoracic and abdominal uncini differ slightly. In M. caspica there are about 4–6 rows of increasingly smaller teeth above the main fang in the thoracic uncini, whereas in M. danubialis n. comb. there are a maximum of 4 rows. The number of teeth per row is also somewhat lower in the species from the Danube. The abdominal uncini in M. caspica have a maximum of 6 rows of teeth, in M. danubialis there are 6–8 rows. Furthermore, the transitional uncini of M. caspica have considerably more apical teeth than those of M. danubialis n. comb.

The distribution area and habitat are also useful for distinguishing Manayunkia species, as shown, for example, by the niche differentiation of the three species from Lake Baikal and the geographical distribution of the two species from North America ( Atkinson et al. 2020, Sitnikova et al. 1997), because the distribution areas of the species are, as far as is known, relatively limited (see Introduction).

Manayunkia caspica has been described on silty bottoms in the Caspian Sea at depths between 17 m and 64 m and salinities between 1.3 and 13.2 psu ( Annenkova 1929a, b). The specimens of Manayunkia that occur in the Danube inhabit a completely different habitat. They live in freshwater, do not tolerate large fluctuations in salinity, prefer oxygen-rich and rocky habitats at shallow depths ( Popescu-Marinescu 2008). Based on the ecological species concept, the spatially and ecologically separated populations from the Caspian Sea and the Danube can therefore also be regarded as distinct species. Genetic studies will ultimately have to clarify whether they are actually separate species.

There is a slight difference in the number of thoracic and abdominal uncini between smaller and larger individuals. Smaller individuals have fewer uncini in general (see also the Remarks on M. danubialis n. comb.).

Two characters in this species requires special attention. This is the presence of transitional uncini in a number of specimens and of a brood chamber in females. Transitional uncini or transitional chaetae on the neuropodia of the last three thoracic chaetigers have been described several times in some species of the Fabriciidae (see Bick 2020, Bick & Armendáriz, 2021). The transitional chaetae are elongated hooded chaetae bent almost at right angles. The upper side of these chaetae bears a multitude of small teeth. This type was first described in Brandtika spp. as ‘pilose chaetae’ ( Jones 1974) and later in M. occidentalis and M. speciosa as ‘elongate hooded chaetae’ ( Atkinson et al. 2020). They also occur in M. baicalensis , M. godlewskii and M. zenkewitschii ( Sitnikova et al. 1997) . Transitional uncini are similar to normal thoracic uncini. But the dentate region is somewhat elongated, a distinct main fang is absent and the entire upper surface is covered with a multitude of small equally sized teeth. This type occurs in M. caspica ( Fig. 3G, H ) and M. danubialis n. comb. ( Fig. 7H ), as well as in M. aestuarina , M. athalassia , M. zenkewitschii and Monroika clarae (own observations, Bick 2020, Bick & Armendáriz, 2021). Whether there is indeed a clear separation of the occurrence of these two types of chaetae or whether one type represents an intermediate form in chaetae change during development must be proven by future studies. The presence of these chaetae is probably a sexual dimorphism, as has been clearly shown for M. occidentalis and M. speciosa ( Atkinson et al. 2020) . Whether this really applies to all Manayunkia species or whether these transitional chaetae/uncini can also occur in males is not yet known. It is also unknown whether normal uncini develop first during individual development and are later replaced by transitional chaetae/uncini or whether this is not the case.

The presence of a brood chamber in females has so far only been described for the three species from Lake Baikal ( Sitnikova et al. 1997). Popescu-Marinescu (2008) also described that the body of the females of individuals from the Danube changes in the reproduction period. They become longer, thinner and, what is particularly important in this context, deformed in the posterior part of their body. This can most likely also be interpreted as the formation of a brood chamber (see also description for M. danubialis n. comb., below). The presence of a brood chamber for M. caspica females is shown here for the first time ( Fig. 2F, G ). This brood chamber is formed by wing-like protrusions of the integument of chaetigers 6 and 7. The segment boundaries are no longer visible. This means that brood chambers have been described in the females of 5 species. Together with the tube wall, these wing-like protrusions form the proper brood chamber. An egg was once observed which was apparently attached to the tube wall ( Fig. 2H ).

Geographic distribution. So far only known from the Caspian Sea. Records outside the Caspian Sea in southeast European rivers are questionable. A re-examination of specimens from these regions, including molecular methods, is urgently required.

Biology. In the material we received from October 2018, there were females with eggs in chaetiger 4, deposited eggs in tubes and juvenile specimens with a length of slightly more than 1 mm. The eggs had a size of about 200– 300 µm x 70–96 µm. It is therefore not possible to make a reliable statement about the reproduction period of this species.

Ecology. This species was first found on silty bottoms from depths between 17 and 64 m and salinities between about 1.3 to 13.2 psu ( Annenkova 1929a, b).

Figures

FIGURE 2. Manayunkia caspica Annenkova, 1929, SEM micrographs. A. Total view of a complete specimen, ventro-lateral view. B. Anterior end, ventral view. C. Anterior end, dorsal view. D. Outside of a flexible tube consisting of finest sediment particles and mucus. E.Anterior end up to chaetiger 3, ventral view. F. Brood chamber on chaetigers 6 and 7. G. Posterior margin of the brood chamber on segment 7. H. Isolated egg from a female tube. I. Posterior end with last thoracic chaetiger (=chaetiger 8) and first abdominal chaetiger (=chaetiger 9), lateral view. Scale bars. A, F, G, I 200 µm, B, C, H 50 µm, D, E 100 µm (abbr: apr anterior peristomial ring, ch1,8,9 chaetiger 1,8,9, fg faecal groove, ppr posterior peristomial ring, vvfa unbranched ventral vascularized filamentous appendages).

FIGURE 3. Manayunkia caspica Annenkova, 1929, SEM micrographs. A. Notopodium of chaetiger 3 with long narrowly hooded and pseudospatulate chaetae. B. Long narrowly hooded chaetae of chaetiger 3. C. Pseudo-spatulate chaetae of chaetiger 3. D–F. Thoracic uncini, different views. G–H. Transitional uncini of posterior thoracic neuropodia. I. Abdominal narrowly hooded chaetae. K. Abdominal uncini of chaetiger 9. Scale bars. A, B, I 10 µm, C–H, K 5 µm.

FIGURE 4. Manayunkia caspica Annenkova, 1929, semithin sections (1 µm) through radiolar crown. A. Branches of radioles and ventral vascularized filamentous appendages, all separated. B. Branches of ventral and median radioles start to fuse (110 µm basal of section A). C. Fusion of branches of ventral and median radioles continues, dorsal radioles still separated; dorsal lips visible (30 µm basal of section B; note: dorsal radiole of the right and left half of the radiolar crown lettered). D. Ventral and median radioles fused, dorsal radioles and dorsal lips separated (12 µm basal of section C). E. Radioles fused, and connected to ventral vascularized filamentous appendage by dorsal lips, except left dorsal radiole (10 µm basal of section D). F. Radioles completely fused, ventral anterior peristomial ring lobe visible (30 µm basal of section E). Scale bars A–F 100 µm (abbr: dl dorsal lips, dr dorsal radiole, mr median radiole, v aprl ventral anterior peristomial ring lobe, vr ventral radiole, vvfa ventral vascularized filamentous appendages).

FIGURE 5. Manayunkia caspica Annenkova, 1929, semithin sections (1 µm) through base of radiolar crown. A. Base of radiolar crown, branchial heart dorsally. B. Cross-section through the peristomial region lobe with cerebral ganglion and peristomial eyes (28 µm basal of section A). Scale bars A, B 100 µm (abbr: aprl anterior peristomial ring lobe, bh branchial heart, cg cerebral ganglion, fg faecal groove, np nephropore, oe oesophagus, pe peristomial eye, vvfa ventral vascularized filamentous appendages).

FIGURE 7. Manayunkia danubialis Băcescu, 1944 n. comb., SEM micrographs. A. Notopodium of chaetiger 1 with short and long, narrowly hooded chaetae. B. Notopodium of chaetiger 2 with pseudo-spatulate and long narrowly hooded chaetae. C. Pseudo-spatulate chaetae of chaetiger 3. D. Inferior thoracic notochaetae of chaetiger 7. E. Abdominal neurochaetae of chaetiger 9. F. Thoracic uncini of chaetiger 2. G. Thoracic neuropodium of chaetiger 3; note the slightly offset arrangement of uncini. H. Transitional uncini of chaetiger 8. I. Abdominal uncini of chaetiger 9. Scale bars. A, B 20 µm, C–E, I 5 µm, F, H 2 µm, G 10 µm.