Epitokous metamorphosis, reproductive swimming, and early development of the estuarine polychaete, Neanthes glandicincta Southern, 1921 (Annelida, Nereididae) on the east coast of the Malay Peninsula

Abstract

The reproductive and developmental characteristics of the nereidid polychaete, Neanthes glandicincta Southern, 1921, commonly recorded in tropical estuaries in the Indo-West Pacific, were examined from Malaysia (the mangrove area of Kuala Ibai, Terengganu) and Thailand (the Lower Songkhla Lagoon) on the east coast of the Malay Peninsula. Epitokous metamorphosis of fully mature males and females and their reproductive swimming behaviour were recorded based on ten Malaysian epitokous specimens, which were collected at night during spring tides in a period of January 2018 to March 2019. Six Thailand epitokes were obtained in February and March 2006 by the laboratory rearing of immature worms. Epitokous metamorphosis is characterised by the enlargement of eyes in both sexes, division of the body into three parts and modification of parapodia with additional lobes in the mid-body of males, and replacement of atokous chaetae in the mid-body by epitokous natatory chaetae, completely in males and incompletely in females. The diameter of coelomic unfertilised eggs in females was 100-140 µm. After fertilisation, each egg formed a jelly layer, inside which embryonic development progressed. Trochophores hatched out of the jelly layer, entering a short free-swimming larval phase followed by demersal life at the early stage of 3-chaetiger nectochaeta one day after fertilisation. Then, the larvae entered benthic life as juveniles, crawling on the bottom, at the late stage of 3-chaetiger nectochaeta two days after fertilisation. The results indicate that N. glandicincta has an annual life cycle, which is usually completed within an estuary with limited larval dispersal ability.

Keywords: Kuala Ibai; Songkhla Lagoon; South China Sea; natatory chaetae; pelagic larvae; trochophore.

Figure 1.

Map showing the collection sites (closed circles) in two estuaries on the east coast of the Malay Peninsula A lower Songkhla Lagoon, Thailand B mangrove area in Kuala Ibai branched from Sungai Ibai in Terengganu, Malaysia.

Figure 2.

Atokes (A–F) and an epitoke (G) of Neanthes glandicincta (Southern, 1921) collected from the Lower Songkhla Lagoon, Thailand A prostomium of an atoke (ind. no. 10 with BW of 1.7 mm, PMBC 21209) B anterior view of an everted proboscis, showing a pair of small nipple-like round papillae on area VI in an atoke (ind. no. SL-2 with BW of 1.5 mm, PMBC 21212) C–F paragnaths in areas I (C), II (anterior and middle parts of left side, D), III (central part, E), and IV (right side, F) of an atoke (ind. no. 1 with BW of 2.3 mm, PMBC 21209) G dorsal (upper) and ventral (lower) views of the right jaw of a male epitoke (ind. no. 3M with BW of 1.2 mm, PMBC 20732).

Figure 3.

Epitokous males (A, C) and females (B, D) of Neanthes glandicincta (Southern, 1921) collected from the Lower Songkhla Lagoon, Thailand (PMBC 20732) in comparison with an atoke from the same locality (E) (PMBC 21209) A dorsal view of the whole body of a male B dorsal view of the anterior body of a female C–E enlargement of anterior dorsal end of a male epitoke (C), a female epitoke (D), and an atoke (E). Scale bars: 5 mm (A, B); 0.5 mm (C–E).

Figure 4.

Male epitoke of Neanthes glandicincta (Southern, 1921) collected from Kuala Ibai, Malaysia (UMTAnn 453) A dorsal view of the whole body (incomplete, with the pre-natatory and natatory regions) B dorsal view of the proboscis with pigmentation C ventral view of the proboscis with pigmentation. Scale bars: 1 mm (A); 0.5 mm (B, C).

Figure 5.

Female epitoke of Neanthes glandicincta (Southern, 1921) collected from Kuala Ibai, Malaysia (UMTAnn 449) A dorsal view of the whole-body B enlargement of anterior end C enlargement of eyes D rupture of body wall at the ventral surface in the posterior body (arrow). Scale bars: 1 mm (A); 0.5 mm (B–D).

Figure 6.

Drawings of epitokes of Neanthes glandicincta (Southern, 1921) collected from Kuala Ibai, Malaysia A posterior view of the right parapodium 8 in the pre-natatory region of a male (UMTAnn 453) B posterior view of the right parapodium 35 in the natatory region of a male (UMTAnn 445) C anterior view of the left parapodium 35 of a female (UMTAnn 449) D posterior view of the right parapodium 66 in the post-natatory region of a male (UMTAnn 446) E heterogomph spiniger from the lower neurochaetae in chaetiger 8 of a male (UMTAnn 453) F homogomph spiniger from the upper neurochaetae in chaetiger 8 of a male (UMTAnn 453) G heterogomph falciger from the lower neurochaetae in chaetiger 36 of a female (UMTAnn 449) H epitokous natatory chaeta from the neuropodium of chaetiger 36 of a male (UMTAnn 453). Scale bars: 1 mm (A–D); 0.05 mm (E–H).

Figure 7.

Epitokous males (A, B, E) and a female (C, D) of Neanthes glandicincta (Southern, 1921) collected from the Lower Songkhla Lagoon, Thailand (PMBC 20732) A anterior view of left parapodium of chaetiger 5 in the pre-natatory region of a male epitoke B anterior view of right modified parapodium of chaetiger 34 in the natatory region of the same male as (A) C posterior view of right parapodium of chaetiger 3 of a female epitoke D posterior view of right parapodium of chaetiger 37 of the same female as (C) E enlargement of an epitokous paddle chaeta of another male epitoke. Abbreviations: dc, dorsal cirrus; vc, ventral cirrus. Scale bars: 0.1 mm (A, C); 0.5 mm (B, D); 0.05 mm (E).

Figure 8.

Seasonal changes of environmental parameters in Kuala Ibai, Malaysia during the sampling period A monthly changes in the salinity and temperature of the surface water at the sampling site (represented by our data at the end of each month) B monthly changes in the amount of rainfall and average air temperature at Kuala Ibai based on the data of Malaysian Meteorological Department C monthly changes of the maximum height of sea level at high tide (closed circles), with the height of sea level at high tide on each sampling date (x marks), based on the data of Worldwide Tides and Currents Predictor (2018). The asterisks indicate the months when the swimming epitokes of Neanthes glandicincta appeared.

Figure 9.

Early development of Neanthes glandicincta (Southern, 1921) after fertilisation in the laboratory. The material from the Lower Songkhla Lagoon, Thailand A fertilised egg surrounded by a jelly layer (j), 10 min after fertilisation; many sperm were trapped in the jelly layer; lipid (oil) drops (o) surrounded the germinal vesicle B 4-cell stage, 1 h and 10 min after fertilisation C early trochophore stage, 7 h and 30 min after fertilisation; ciliary movement of the prototroch (p) began within the jelly layer D free-swimming trochophore larva just after hatching out of the jelly layer, 8 h after fertilisation; ciliary bands of the prototroch and telotroch (t) were present E free-swimming early-metatrochophore larva, 20 h after fertilisation; two pairs of chaetal tufts (c) were present F free-swimming 2-chaetiger late-metatrochophore larva, 21 h after fertilisation; two pairs of chaetal tufts well developed G free-swimming early 3-chaetiger nectochaeta larva, 22 h after fertilisation; three pairs of chaetal tufts were developed; the prototroch and lipid drops remained in the anterior body H demersal late 3-chaetiger nectochaeta larva, 48 h after fertilisation; a pair of eyes (e), antennae (a), and anal cirri (ac) appeared. Lipid drops disappeared. Scale bars: 0.2 mm.