Sinonereis heteropoda Wu & Sun 1979

Sinonereis heteropoda Wu & Sun, 1979 (Figs 1-3)

Sinonereis heteropoda Wu & Sun, 1979: 96, figs 1a-j, 2a-d. — Wu et al. 1985: 52-54, figs 1A-J, 2A-D. — Sun & Yang 2004: 80-82, fig. 3 A-N.

Nicon sinica Wu & Sun, 1979: 99 -101, fig. 3a-j, n. syn. — Wu et al. 1985: 60-61, fig. 3 A-J. — Miura 1990: 11-14, figs 1a-i, 2a-j. — Paik 1997: 154, fig. 2a-j. — Sun & Yang 2004: 79-80, fig. 3 A-J.

TYPE MATERIAL OF S. HETEROPODA. — Holotype. China, Yellow Sea, MBMCAS A-36, ♂, R/ V Handan, collection No. H 0038-28, St. 3031 (36°00N, 121°00E), 30 m, mud and gravel, 27.I.1959.

Paratypes. China, East China Sea. MBMCAS A-37 (1), ♂, R/V 401, Collection No. D 14 B-1, St. 4083 (28°00N, 123°30E), 90 m, fine brown sand, 8.XII.1959. — China, South China Sea. MBMCAS A-38 (1), ♂, R/V 101, collection No. N 19 B-19, St. 6060 (22°00N, 113°36E), 93 m, mud and sand, 7.V.1960.

TYPE MATERIAL OF N. SINICA. — Holotype. China, Yellow Sea, MBMCAS A-39, R/ V Yancheng, collection No. Y 28 B-5B, St. 3031, 29 m, brown sand and gravel, 13. VI.1959. — Paratype. China, South China Sea. MBMCAS A-41 (1), R/ V Hanggong, collection No. K 6 B-4, St. 0 79 (20°00N, 113°00E), 117 m, mud and sand, 11.VII.1959.

DISTRIBUTION. — Yellow Sea; East China Sea; South China Sea; Pacific Ocean off Honsu, Japan.

DESCRIPTION OF EPITOKE

Body

Holotype of Sinonereis heteropoda (MBMCAS A-36) male, complete with 60 chaetigers, 12.6 mm long, 1.5 mm wide at chaetiger 10 (including parapodia); paratype (MBMCAS A-37) male, complete with 60 chaetigers, fragmented into two parts, anal cirri missing, 12.5 mm long, 1.5 mm wide at chaetiger 10. Body yellowish, tapering posteriorly, pigmentation absent (Fig. 2 A-C); whitish bundles of sperm in coelom present.

Anterior end

Prostomium ovate, wider than long; two independent antennae, half as long as prostomium; palps biarticulated, as long as antennae; eyes black, ovate to reniform, subequal (Figs 1A; 2A, B). Achaetous ring twice longer than first chaetiger; anterior cirri smooth, posterodorsal one reaching chaetiger 14 (Figs 1A, 2A). Jaws transparent, brownish, dentate, each jaw with 7-8 teeth (Fig. 2 D-E); pharynx smooth (Figs 1A; 2D, E).

Chaetigers

Body divided into non-natatory and natatory regions. Nonnatatory region subdivided in three subregions: a) chaetigers 1-4 with dorsal cirri fusiform and ventral cirri cirriform; b) chaetigers 5-7 with dorsal cirri napiform and ventral cirri fusiform; and c) chaetigers 8-21 with both dorsal and ventral cirri cirriform. Natatory region from chaetiger 22 to end of body.

First two chaetigers with neuroaciculae only, following chaetigers with both noto- and neuroaciculae. In chaetiger 1, dorsal cirrus cirriform, 1.5 times longer than dorsal ligule. Dorsal ligule digitiform, twice as long as neuroacicular ligule. Neuroacicular ligule subconical; postchaetal lobe digitate, 1.5 times longer than neuroacicular ligule; neuropodial ventral ligule digitate, as long as dorsal ligule. Ventral cirrus cirriform, half as long as neuropodial ventral ligule.

In chaetiger 3 (Fig. 1B), dorsal cirrus fusiform (i.e., cirrophore slightly swollen, cirrostyle distinct), two times as long as notopodial ventral ligule. Notopodial dorsal ligule absent; prechaetal lobe inconspicuous; notopodial ventral ligule digitate, as long as neuropodial postchaetal lobe. Neuroacicular ligule subconical, half as long as postchaetal lobe; postchaetal lobe digitate; neuropodial ventral ligule digitate, as long as postchaetal lobe. Ventral cirrus cirriform, half as long as neuropodial ventral ligule.

In chaetigers 5-7 (Fig. 2H, I), dorsal cirrus with cirrophore globose or ovoid, cirrostyle cirriform. Notopodial dorsal ligule digitate, half as long as dorsal cirrus, as long as notopodial ventral ligule; prechaetal lobe rounded, very small; notopodial ventral ligule digitate, twice longer than neuroacicular ligule. Neuroacicular ligule subconical; postchaetal lobe digitate, slightly longer than neuroacicular ligule; neuropodial ventral ligule digitate, as long as neuroacicular ligule. Ventral cirrus fusiform, 0.8 times as long as neuropodial ventral ligule.

In chaetigers 8-21, dorsal and ventral cirri slender, cirriform. Notopodial and neuropodial ligules similar as in chaetigers 5-7.

Chaetigers from 22 to end of body modified (Fig. 2 J-K). Dorsal cirrus with cirrophore slightly swollen, cirrostyle cirriform, 1.3 times length of notopodial dorsal ligule, becoming as the same length toward posterior chaetigers; dorsal lamella twice larger than cirrophore of dorsal cirrus. Notopodial dorsal ligules subconical, as long as notopodial ventral ligule; prechaetal lobe rounded, small; notopodial ventral ligule subconical or digitate, twice as long as neuroacicular ligule. Neuroacicular ligule subconical; postchaetal lobe expanded, lamellar, as long as and as wide as neuroacicular ligule, becoming shorter toward posterior chaetigers, tip with a small apex; neuropodial ventral ligule digitate, twice as long as neuroacicular ligule. Ventral cirrus cirriform, 0.8 times as long as neuropodial ventral ligule, with two small basal lamellae, becoming inconspicuous toward posterior chaetigers.

Chaetae

Notochaetae homogomph spinigers. Neurochaetae homogomph spinigers and heterogomph falcigers in supraacicular fascicles (Fig. 2F); heterogomph spinigers and falcigers in sub-acicular fascicles (Fig. 2G). Natatory chaetae absent.

Notopodial and neuropodial homogomph spinigers pectinate, teeth decreasing in size toward distal end; neuropodial heterogomph spinigers pectinate, teeth decreasing in size toward distal end, blade shorter than homogomph ones (Fig. 2F, G). Neuropodial heterogomph falcigers pectinate, teeth minute, distal tooth stout, incurved, with a distal tendon, both supra- and sub-acicular falcigers similar in size and shape in the same chaetiger; blades of falcigers increasing in size, teeth increasing in number, and size of both distal tooth and tendons decreasing in size, toward posterior chaetigers (Fig. 2F, G).

Posterior end

Pygidium tripartite; anal cirri cirriform, as long as last eight chaetigers (Fig. 2A, insert).

DESCRIPTION ATOKE

Body

Holotype of Nicon sinica (A-39) atoke specimen with 51 chaetigers, 11.5 mm long, 1.2 mm wide at chaetiger 10; paratype (A-41) immature with 48 chaetigers, 12 mm long, 1.4 mm wide at chaetiger 10. Body yellowish, tapering posteriorly; brown pigment spots in prostomium and palps, brown spots in anterior margin of anterior chaetigers aligned in a band, fading in most-posterior chaetigers. Glandular masses brown at the base of dorsal cirri, both notopodial dorsal and ventral ligules, and neuropodial ventral ligules, in first third of body, enhancing toward posterior chaetigers; glandular masses in neuropodial ventral ligules disappearing toward posterior chaetigers.

Anterior end

Prostomium subpyriform, as long as wide; two independent antennae, half as long as prostomium; palps biarticulated, as long as antennae; eyes black, rounded, subequal (Fig. 3A, B). Achaetous ring twice longer than first chaetiger; anterior cirri smooth, posterodorsal one reaching chaetiger 14 (Fig. 3 A-C). Jaws dentate, each with 6-7 teeth; pharynx bare (Fig. 3E).

Chaetigers

First two chaetigers with neuroacicula only, following ones with both noto- and neuroaciculae. In chaetiger 3 (Fig. 3H), dorsal cirri cirriform, 1.5 times longer than dorsal ligule. Notopodial dorsal ligule absent; prechaetal lobe inconspicuous; notopodial ventral ligule digitate, 1.5 times longer than neuroacicular ligule. Neuroacicular ligule digitate, twice longer than postchaetal lobe; postchaetal lobe subconical, half as long as neuropodial ventral ligule; neuropodial ventral ligule digitate. Ventral cirrus cirriform, 0.6 times as long as neuropodial ventral ligule.

In chaetiger 7 (Fig. 3I), dorsal cirrus cirriform, 0.8 times as long as notopodial dorsal ligule. Notopodial dorsal ligule subconical, as long as notopodial ventral ligule; prechaetal lobe rounded, small; notopodial ventral ligule subconical, 1.5 times length of neuroacicular ligule. Neuroacicular ligule subconical, as long as neuropodial ventral ligule; postchaetal lobe digitate, as long as neuroacicular ligule; neuropodial ventral ligule subconical. Ventral cirrus cirriform, 0.6 times as long as neuropodial ventral ligule.

In chaetigers 19 and 39 (Fig. 3 J-K), dorsal cirrus cirriform, 0.8 times as long as notopodial dorsal ligule. Notopodial dorsal ligule subconical, 0.8 times as long as notopodial ventral ligule; prechaetal lobe rounded, small; notopodial ventral ligule subconical, twice as long as neuroacicular ligule. Neuroacicular ligule subconical, 0.8 as long as neuropodial ventral ligule; postchaetal lobe digitate, as long as neuroacicular ligule; neuropodial ventral ligule subconical. Ventral cirrus cirriform, half as long as neuropodial ventral ligule.

Chaetae

Notochaetae homogomph spinigers. Neurochaetae homogomph spinigers and heterogomph falcigers in supra-acicular fascicles; heterogomph spinigers and falcigers in sub-acicular fascicles. Notopodial and neuropodial homogomph spinigers pectinate, teeth decreasing in size toward distal end; neuropodial heterogomph spiniger pectinate, teeth decreasing in size toward distal end, blade shorter than homogomph ones (Fig. 3F). Neuropodial heterogomph falcigers pectinate, teeth minute, distal tooth stout, incurved, with a distal tendon, increasing in size toward posterior chaetigers (Fig. 3G); both supra-and sub-acicular falcigers similar.

Posterior end

Pygidium tripartite; anal cirri cirriform (one missing in holotype), as long as last four chaetigers (Fig. 3D).

REMARKS

The examination of the type material revealed a high resemblance between Sinonereis heteropoda and Nicon sinica, mainly in the long anterior cirri, lack of pharyngeal ornamentation, and quite similar parapodial and chaetal morphology, such as the unusual start of the notopodial dorsal ligules from chaetiger 4, as well as the progressive change of the blade shape in neuropodial falcigers. Wu & Sun (1979) likely overlooked these high similarities because they focused on the modification of dorsal cirri in chaetigers 5-7 in S. heteropoda, which were absent in the epitokes of Nicon species described in their study, N. maculata and N. moniloceras (Wu & Sun 1979). The examined material differs slightly from those of Miura (1990) mainly in the size of the cirrophores of dorsal cirri in chaetigers 5-7, and the size of the lamellae in natatory chaetigers, particularly in those joined to the ventral cirri. This difference might reflect changes during the process of transformation. Núñez et al. (2000) reported Nicon sinica from Cape Breton Canyon, Cantabrian Sea, at 917-954 m depth and compared their specimens with those described from Japan, and later Núñez (2004) identified the specimens as Sinonereis heteropoda. Núñez et al. (2000) highlighted the lack of pigmentation and higher amount of notopodial homogomph spinigers (23-52) in chaetiger 10, whereas the Japanese specimens have pigmentation and a lower amount of such spinigers (9-15) (Núñez et al. 2000: 32). There are additional differences: in Chinese specimens the posterodorsal pair of anterior cirri reach chaetiger 14, in chaetiger 10 both notopodial dorsal and ventral ligules are subequal and the ventral cirrus is half as long as neuropodial ventral ligule; whereas in the specimens from Cape Breton Canyon the posterodorsal pair of anterior cirri reach chaetiger 6, in chaetiger 10 notopodial dorsal ligule is shorter than notopodial ventral one and the ventral cirrus is longer than neuropodial ventral ligule. On the other hand, Gillet & Dauvin (2000) reported Sinonereis sp. in the vicinity of Hyères Seamount at 480-705 m depth in bioclastic sand, sponges and gravel, but they did not include any description or justification. Whether the above two records belong to Sinonereis requires a further study to elucidate their status.

In this contribution, we confirm the proposal of Miura (1990) that the two species belong to different stages of a single species, i.e., S. heteropoda and N. sinica are described based on epitokes and atokes, respectively. The well-defined sexual dimorphism is also emphasized that not only atokes but also females have no heteronereid transformation.

Further, this revision of the type material supports the synonymy of Sinonereis heteropoda and Nicon sinica, but we consider Sinonereis as a separate genus, because epitokal modification is definitely different between Nicon and Sinonereis. The main differences are that epitokes of Nicon species have no napiform dorsal cirri in chaetigers 5-7, and notopodial dorsal ligules start from chaetiger 3. The genera can also be separated by some other characters as shown in Table 1. For instance, heteronereis of N. aestuarensis Knox, 1951 has both upper and lower lamellae of dorsal cirri and a lamella below the notopodial dorsal ligule (Knox 1951), which are all absent in S. heteropoda. Parapodia of natatory region have only a ventral lamellar process in N. maculata Kinberg, 1865 but four modified processes are present in S. heteropoda. Natatory chaetae are present in N. moniloceras (Hartman, 1940) but absent in S. heteropoda (Hartman 1940; Wu & Sun 1979).

Wu & Sun (1979: 96) compared Sinonereis with Leptonereis Kinberg, 1865 because the expanded ‘shape of the dorsal cirri’ and bare pharynx (Kinberg 1865), but they regarded both genera as independent because in Leptonereis such structures are in the posterior chaetigers, whereas in Sinonereis they are in the anterior chaetigers. Wu et al. (1985) noted that the expanded dorsal cirri in Leptonereis species are actually the notopodial dorsal ligules (Hartman 1945) and added the lack of neuropodial postchaetal lobes in Leptonereis and present in Sinonereis, likely they referred to ventral lamellae present in natatory chaetigers of Sinonereis epitokes but absent in the holotype of L. laevis after it consists of an atoke specimen (Hartman 1948). Nevertheless, the expanded notopodial ligules in posterior chaetigers are also absent in the atokes of S. heteropoda, ensuring its separation from L. laevis.

The genus Rullierinereis Pettibone, 1971 is also closely similar to Sinonereis after the bare pharynx and smooth tentacular cirri but a set of both atokous and epitokous features ensure their separation. Atokes of Rullierinereis species have notopodial homogomph falcigers and the notopodial dorsal ligules decrease in size and even disappear toward posterior chaetigers, features absent in atokes of Sinonereis species; further, atokes of Sinonereis have prechaetal notopodial lobes which are absent in Rullierinereis species (Pettibone 1971). Moreover, epitokes of Rullierinereis species have lower lamellae in dorsal cirri, natatory chaetae, and the females transform into heteronereis, whereas all these features are absent in epitokes of Sinonereis species; also, Sinonereis male epitokes have napiform dorsal cirri in chaetigers 5-7, feature absent in Rullierinereis male epitokes (Table 1) (Pettibone 1971). Sinonereis closely re- sembles Kainonereis Chamberlin, 1919 because they have a similar modification of dorsal cirri in chaetigers 5-7 (Chamberlin 1919). However, in Kainonereis the dorsal cirrophores are clearly modified into elytriform structures, namely dorsal discs (Conde-Vela et al. 2018), whilst in Sinonereis corresponding cirrophores are globose or ovoid. Moreover, males of Kainonereis have anterior cirri truly articulated, upper and lower lamellae of dorsal cirri, notopodial homogomph falcigers in first seven chaetigers and well-developed natatory chaetae, all of which are absent in males of Sinonereis (Table 1). In addition, females have similar heteronereid modifications as males in Kainonereis (only lacking the notopodial homogomph falcigers in first seven chaetigers), whereas in Sinonereis females display no heteronereid transformation. The start of notopodial dorsal ligules from chaetiger 4 in males and chaetiger 3 in females is also remarkable in Kainonereis epitokes, whereas in Sinonereis they start from chaetiger 4 in both males and females.

As an additional confirmation of how problematic it is matching atokes and epitokes, we must recall that the atokes of Sinonereis, and atoke and epitokes of some Kainonereis species, were regarded as different species in Nicon because of the simple definitions of these genera. However, the differences among the epitoke specimens belonging to the genera Kainonereis, Nicon and Sinonereis mentioned above allow us to recognize Sinonereis as a distinct, valid genus.

The lack of heteronereid transformations in females has been reported for other nereidid species. Males of Alitta virens (Sars, 1835) undergo epitoky and the heteronereis spawn in front of the galleries of the unmodified females, which trap the sperm by moving the water inside, and after release the oocytes and the eggs and the benthic larvae which are retained inside (Bass & Brafield 1972). Also, there are metabolic differences between males and females because of the energetic requirements for swimming (Chatelain et al. 2008). Similarly, females of Sinonereis heteropoda could remain inside their galleries in the mud and the fecundation could occur inside, and therefore a restricted distribution is expected. Future studies about the ecology, physiology and reproduction of this species are encouraged to elucidate such issues.