Prionospio cf. paucipinnulata Blake & Kudenov, 1978

Radashevsky, Vasily I., 2015, Spionidae (Annelida) from Lizard Island, Great Barrier Reef, Australia: the genera Aonides, Dipolydora, Polydorella, Prionospio, Pseudopolydora, Rhynchospio, and Tripolydora, Zootaxa 4019 (1), pp. 635-694 : 669-673

Prionospio cf. paucipinnulata Blake & Kudenov, 1978

( Figs 22–24 )

Prionospio (Prionospio) paucipinnulata Blake & Kudenov, 1978: 217 –219, fig. 22. Prionospio paucipinnulata .— Hutchings & Murray, 1984: 61.

Material examined. Queensland: AM W.45239, MI QLD 2330a (12); AM W.45240, MI QLD 2357 (1); AM W.45241, MI QLD 2360 (1); AM W.45242, MI QLD 2365 (2); AM W.45243, MI QLD 2373 (6); AM W.45377, MI QLD 2391 (1); AM W.45244, MI QLD 2410 (2); AM W.45245, MI QLD 2410 (4); AM W.45246, MI QLD 2431 (1); AM W.45378, MI QLD 2440 (4); MIMB 28108, MI QLD 2440 (2).

Adult morphology. Up to 13 mm long, 0.3 mm wide for 60 chaetigers; smallest examined individual with 30 chaetigers. Pigmentation in life absent. Prostomium narrow, rounded anteriorly ( Fig. 22 A–C), extending posteriorly to end of chaetiger 4 as a low caruncle, shorter in small individuals ( Fig. 23 B). Five small knobs with short non-motile cilia present on frontal and fronto-lateral edges of prostomium. Occipital antenna absent. Two pairs of eyes present, comprising one pair of small lateral eyes and one pair of median eyes; median eyes small to moderately large in 30–45-chaetiger immature individuals ( Fig. 22 A, D); in larger mature individuals, median eyes very large, overlapping lateral eyes ( Fig. 22 B); eyes red in life, appearing black in many formalin-fixed specimens. Nuchal organs U-shaped ciliary bands on lateral sides of caruncle. Posterior dorsal parts of peristomium fused to notopodial lamellae of chaetiger 1 forming moderate ear-shaped structures ( Fig. 24 A). Palps as long as 10–15 chaetigers, with frontal longitudinal groove lined with fine cilia, short transverse bands of cilia regularly arranged on inner surface, and narrow longitudinal band of cilia running on outer fronto-lateral side along frontal groove on distal half of palp; cilia of inner transverse bands beating towards distal end of palp, while cilia of outer longitudinal band beating towards frontal groove.

Chaetiger 1 with short capillaries and small postchaetal lamellae in both rami; notopodial postchaetal lamellae fused to posterior dorsal parts of peristomium forming moderate ear-shaped structures. Notopodial lamellae of chaetigers 3–5 largest, triangular; lamellae getting gradually smaller and rounded on succeeding chaetigers. Lower part of neuropodial postchaetal lamellae of chaetiger 2 acuminate and elongated ventrally ( Fig. 24 A). Neuropodial lamellae of chaetiger 3 trapezoidal, from chaetiger 4 onwards lamellae rounded, semicircular, diminishing in size on posterior chaetigers ( Fig. 24 A).

Prominent semi-circular dorsal crest joining notopodial lamellae of chaetiger 7 ( Fig. 24 A), when oriented forward, crest overlapping chaetiger 6 and posterior half of chaetiger 5. Low dorsal crests present from chaetiger 8 to chaetigers 16–31 gradually diminishing in size on posterior chaetigers. Lateral pouches and ventral flaps absent. Sabre chaetae in neuropodia from chaetiger 10, one, occasionally two in a group; chaetae with narrow limbation and fine granulation on distal end ( Fig. 24 E).

Hooks in notopodia from chaetigers 20–35 ( Fig. 23 C), up to six in a series among capillaries. Hooks in neuropodia from chaetigers 10–14 ( Fig. 23 C), up to eight in a series, accompanied by inferior sabre chaetae and alternating capillaries throughout. Alternating capillaries thin, with narrow wing in anterior neuropodia, alimbate in posterior chaetigers, 2–3 times as long as hooks. Hooks with outer and small inner hoods, multidentate, with 4–5 pairs of small upper teeth arranged in two vertical rows above main fang; shaft slightly bent ( Fig. 24 D).

Smallest 30-chaetiger individual with three pairs of smooth apinnate branchiae on chaetigers 2–4; individuals up to 45–50-chaetiger stage with pinnate branchiae on chaetiger 2 and smooth branchiae on chaetigers 3–5 ( Fig. 24 B); individuals with 50–55 chaetigers usually with 7–9 pairs of pinnae on each branchia of chaetiger 2, 4–6 pairs of pinnae on each branchia of chaetiger 4, and smooth branchiae on chaetigers 3 and 5 ( Fig. 24 A, C); larger individuals with up to 12 pairs of pinnae on each branchia of chaetiger 2, 2–4 pairs on each branchia of chaetiger 3, and 5–7 pairs on each branchia of chaetiger 4; branchiae on chaetiger 5 smooth, apinnate ( Fig. 23 A). In large individuals, branchiae on chaetiger 2 longest, 3–5 times as long as notopodial lamellae; branchiae on chaetiger 3 about half of length of those on chaetiger 2; branchiae on chaetiger 4 up to 2/3 of length of those on chaetiger 2, and branchiae on chaetiger 5 equal or slightly shorter than those on chaetiger 3. All branchiae cylindrical to slightly flattened antero-posteriorly, with longitudinal bands of cilia running along inner and outer edges. Pinnae short, regularly arranged in two rows on postero-lateral sides of branchiae leaving basal parts about 1/5 and distal parts 1/ 4 free from pinnules. Afferent and efferent blood vessels interconnected by numerous radial blood capillaries giving branchiae annulate appearance; radial capillaries making loops inside pinnae.

Nototrochs present between branchial bases, each composed of one row of short cilia. Dorso-lateral longitudinal ciliation present on chaetigers 3–6 as short bands of dense cilia extending between successive notopodia.

Pygidium with one long middorsal cirrus and a pair of shorter ventral cirri.

Oesophagus extending through 5–7 anterior chaetigers. Ventral buccal bulb below oesophagus extending to end of chaetiger 1. Gizzard-like structure in digestive tract absent.

Main dorsal blood vessel transformed into gut sinus in anterior part of midgut. Soft heart body up to 20 µm in diameter extending inside main dorsal vessel from level of chaetigers 3–4 to chaetigers 9–11. Blood red, without globules or other elements.

Nephridia in small individuals in chaetigers 4–5, in large individuals in chaetigers 4–6 ( Fig. 23 B), large and greenish in chaetiger 4, smaller and less pigmented to transparent in chaetiger(s) 5 (6).

Reproduction. Prionospio cf. paucipinnulata is gonochoristic. Both in female and males gametes develop from chaetiger 10 through most part of body. Oogenesis is intraovarian. Vitellogenic oocytes develop in ovaries attached to segmental blood vessels. Intraovarian oocytes were up to 100 µm in diameter, with germinal vesicle about 45 µm and single nucleolus 17 µm in diameter. Oocyte envelope is 1.5–2 µm thick, smooth, with single depression about 13 µm in diameter and 10–13 µm deep. Spermatogonia proliferate in testes; spermatogenesis occurs in the coelomic cavity. Spermatids are joined in tetrads. Spermatozoa are ect-aquasperm with small acrosome, spherical nucleus 2–3 µm in diameter, spherical mitochondria probably four in number, and a long flagellum.

Remarks. Prionospio from Lizard Island with 30–60 chaetigers having sabre chaetae from chaetiger 10, prominent dorsal crest on chaetiger 7 and low crests on succeeding chaetigers showed significant variation of other taxonomic morphological characters as it described above. This variation is herein explained by transformation of characters during ontogenesis. It is suggested that median eyes enlarge greatly at 45–50-chaetiger stage apparently in association with sexual maturation of an individual. Branchiae develop successively from chaetiger 2 to chaetiger 5, and pinnae appear first on the first pair of branchiae when only two or three pairs of branchiae are developed. After development of the fourth pair of branchiae on chaetiger 5, pinnae begin to appear on the third pair of branchiae and later on the second pair. As growth proceeds, hooks are gradually lost from neuropodia until chaetiger 14 and from notopodia until chaetiger 35. Sabre chaetae retain their anterior position on chaetiger 10 during entire life span.

Mid-size, 45–55-chaetiger Prionospio from Lizard Island appear similar to P. paucipinnulata Blake & Kudenov, 1978 which was originally described from Port Phillip Bay, Victoria, Australia. Blake & Kudenov (1978) noticed small size of adults, up to 7 mm long for 53 chaetigers, and described them as having caruncle extending to end of chaetiger 4, large red median eyes, chaetiger 1 with capillaries in both rami, chaetiger 2 with small rounded neuropodial lamellae, pinnate branchiae on chaetigers 2 and 4, smooth branchiae on chaetigers 3 and 5, prominent dorsal crest on chaetiger 7 and low crest on chaetiger 8, sabre chaetae in neuropodia from chaetiger 10, and hooded hooks with 3–4 pairs of upper teeth, beginning in notopodia from chaetigers 34–35 and in neuropodia from chaetiger 13. Large Prionospio from Lizard Island have pinnae on the first three pairs of branchiae and thus differ from the original description of P. paucipinnulata . It may be, however, that Blake & Kudenov (1978) described an intermediate stage of the development of P. paucipinnulata , and in larger worms from Victoria pinnae develop on the second pair of branchiae (on chaetiger 3) same as in large worms (with 55–60 chaetigers) from Queensland. The number of branchial pinnae and the arrangement of hooks in noto- and neuropodia in P. paucipinnulata is within the range of those characters in Prionospio from Lizard Island. Two characters, neuropodial lamellae of chaetiger 2 and dorsal crests (as they were described by Blake & Kudenov 1978) are, however, different in the two groups of worms. According to the original description, P. paucipinnulata has small rounded neuropodial lamellae on chaetiger 2, and a low crest only on chaetiger 8, whereas Prionospio from Lizard Island have acuminate and ventrally elongated neuropodial lamellae on chaetiger 2, and low crests from chaetiger 8 to 20–30th chaetigers.

After Blake & Kudenov (1978), Hutchings & Murray (1984) reported P. paucipinnulata from New South Wales, and Dagli & Çinar (2010) suggested introduction of the species to the Aegean and Levantine coasts of Turkey with ballast waters of ships. The latter authors described worms 5.9 mm long for 45 chaetigers and having pinnate branchiae on chaetigers 2 and 4 and apinnate branchiae on chaetigers 3 and 5. They also noticed small rounded neuropodial lamellae on chaetiger 2, but in addition to the prominent dorsal crest on chaetiger 7 described low crests arranged from chaetiger 8 to chaetiger 16.

Completely developed 55–60-chaetiger Prionospio from Lizard Island appear similar to P. ergeni originally described from the Levantine Sea by Dagli & Çinar (2009). Worms in both groups are unique among Prionospio in having three pairs of pinnate branchia on chaetigers 2–4 and one pair of apinnate branchiae on chaetiger 5. Only incomplete specimens were available for the original description of P. ergeni , thus it is impossible to estimate the size of the complete worms. Remarkably, however, adult P. ergeni appear quite similar to adult P. paucipinnulata from Turkey decsribed by Dagli & Çinar (2010). Worms in both groups have large median eyes, small rounded neuropodial lamellae on chaetiger 2, sabre chaetae in neuropodia from chaetiger 10, and hooded hooks with 4–5 pairs of small upper teeth above main fang. They differ from each other mainly in the presence of pinnate branchiae on chaetiger 2 in worms of the former group and apinnate branchiae in the latter. More posterior start of hooks in neuropodia in P. e rge n i (from chaetigers 16–18) than in P. paucipinnulata from Turkey (from chaetiger 13) may indicate larger size of the former worms (hooks gradually lost in neuropodia with age in many Prionospio species), while earlier start of hooks in notopodia in P. e rge n i (from chaetiger 30) than in P. paucipinnulata from Turkey (from chaetigers 32–33) may result from limited observations by the authors (arrangement of hooks in notopodia in Prionospio worms is always size-dependent and usually variable even among same-size individuals). Comparison of caruncle length in P. e rge n i and P. paucipinnulata from Turkey is also confusing. Dagli & Çinar (2009: 7) noticed that in P. ergeni “caruncle extending to chaetiger 2” (meaning end of chaetiger 1—VIR) but depicted caruncle to middle of chaetiger 3 ( Dagli & Çinar 2009: fig. 3B) and SEM illustrated caruncle extending apparently to end of chaetiger 3 ( Dagli & Çinar 2009: fig. 4).

Taking into account succession of the development of pinnae on branchiae in Prionospio from Lizard Island (first on the first pair of branchiae, then on third and ultimately on second pair of branchiae) and loss of hooks in parapodia with age in Prionospio , differences described by Dagli & Çinar (2009, 2010) between P. ergeni and P. paucipinnulata from Turkey may be explained by ontogeny and the two groups of worms may belong to the same species. This species may actually be different from P. paucipinnulata from Victoria, Australia in the shape of neuropodial lamellae on chaetiger 2, if small rounded lamellae will not be confirmed in the Australian specimens. If P. paucipinnulata from Victoria do have small rounded neuropodial lamellae on chaetiger 2, Prionospio from Lizard Island described herein should be referred to a new species because these worms have lamellae on chaetiger 2 with lower part acuminate and elongated ventrally.

Further examination of P. paucipinnulata from Victoria, Australia is needed to clarify the morphology of branchiae and neuropodial lamellae of chaetiger 2 in completely developed individuals. Pending such examination, worms from Lizard Island are herein referred to as P. cf. paucipinnulata .

Habitat. In this study, adults of P. cf. paucipinnulata were found in fine sand on the intertidal and at 14 m depth.

Distribution. Australia: Victoria, New South Wales,? Queensland.

Figures

FIGURE 22. Prionospio cf. paucipinnulata. A, B—AM W. 45239; C, D—AM W. 45243; E, F—AM W. 45247. A – C. Anterior ends, dorsal view, showing eyes of various shapes; D. Anterior end, left lateral view; E, Anterior end, dorsal view, showing branchiae with few pinnae on chaetiger 2 and apinnate branchiae on chaetigers 3 and 4; F. Chaetigers 4 - 8, dorsal view, showing apinnate branchiae on chaetiger 5 and prominent dorsal crest on chaetiger 7 overlapping chaetiger 6. Scale bars: A, B, D – F— 50 µm; C— 100 µm.

FIGURE 23. Prionospio cf. paucipinnulata. A. Relationships between shape of branchiae (smooth (s) or pinnate (p )) on a particular chaetiger (chaetigers 2 – 5) and total number of chaetigers in worm; B. Relationships between caruncle length (in chaetiger numbers) and total number of chaetigers in worm, and posterior position of excretory metanephridia (referring to number of the last chaetigers bearing nephridiopores) and total number of chaetigers in worm; C. Relationships between anterior position of hooks in neuro- and notopodia (in chaetiger numbers) and total number of chaetigers in worm.

FIGURE 24. Prionospio cf. paucipinnulata. A, D, E—AM W. 45377; B, C—AM W. 45243. A. Anterior end, left lateral view; B. Set of branchiae on chaetigers 2 – 5 of a 45 - chaetiger individual; C. Set of branchiae on chaetigers 2 – 5 of a 50 - chaetiger individual; D, E. Neurochaetae from a middle chaetiger; D. Multidentate hooded hook; E. Inferior sabre chaeta.