Revision of Sinonereis Wu & Sun, 1979 (Annelida: Nereididae)

ABSTRACT The genus Sinonereis Wu & Sun, 1979 and the species Sinonereis heteropoda Wu & Sun, 1979 were described from Chinese waters, based on only epitokous specimens with modified dorsal cirri in chaetigers 5-7 and bare pharynx. In the same publication, another species based on only atokes was described, Nicon sinica Wu & Sun, 1979. We show that N. sinica is a junior synonym of S. heteropoda based on their affinities in chaetal and parapodial features. We redefine Sinonereis and formally synonymize N. sinica and S. heteropoda. Sinonereis closely resembles Nicon Kinberg, 1865 and Kainonereis Chamberlin, 1919, but Sinonereis differs from them by having napiform dorsal cirri in chaetigers 5-7, and by lacking notopodial dorsal ligules in chaetiger 3 in both atokes and epitokes.


INTRODUCTION
Epitoky in nereidids consists in several morphological and physiological changes for a short pelagic life for reproduction, where the modified adults or epitokes swim and release their gametes in the water column; the unmodified individuals prior the sexual maturity are called atokes (Clark 1961;Schroeder & Hermans 1975). The morphological modification often involves changes in parapodial, chaetal and sometimes pharyngeal ornamentation morphology. The linking of the atokes or non-reproductive stage with their respective epitokes of the same species is often difficult. Some genera have been established based on epitokes only because the epitokal modifications are very distinctive, but since the atoke morphology is not known, it is possible that some atoke-based species in different genera are actually the non-reproductive stage of another epitoke-based species; hence the importance of studying both epitoke and atoke morphology of known species (Conde-Vela et al. 2018).
The finding of some nereidid epitokes showing a unique combination of morphological features prompted Wu & Sun (1979: 95, 96) to propose a new genus, Sinonereis to include a new species, S. heteropoda. The morphological features were that the pharynx had no papillae nor paragnaths, and that dorsal cirri of chaetigers 5-7 were modified as a "bulbous base and styliform terminal end". In the same publication, Wu & Sun (1979) also recorded Nicon Kinberg, 1865 in China seas, and described another new species N. sinica based on several atokous specimens. Both species are very similar because they share the same characters of pharynx and chaetae as well as the same distribution range, and the main difference lies in the modified dorsal cirri in chaetigers 5-7 which are absent in N. sinica.
Subsequently, Miura (1990) recorded Nicon sinica in Japanese waters and found the species exhibit well-defined sexual dimorphism based on a number of specimens selected from a single sample. Males had dorsal cirri modified and neuropodial postchaetal lobes, matching the description of S. heteropoda, whereas females and immatures, showing no heteronereid transformations, were readily recognized as N. sinica. Miura (1990) concluded that the two species might belong to different stages of a single species, but he preferred to retain both species as valid instead of elucidating the synonymous status due to the unavailability of the type material.
Sinonereis closely resembles Kainonereis Chamberlin, 1919 because they both have a bare pharynx as well as modified dorsal cirri along chaetigers 5-7, but their affinities have not been assessed, mainly because the latter had not been revised until quite recently (Conde-Vela et al. 2018). In this contribution, we redescribe S. heteropoda based on the type material. Also, the synonymy of N. sinica with S. heteropoda is addressed, and the relationship between Sinonereis and Kainonereis, and also other similar genera, is discussed.

MATERIAL AND METHODS
Type materials of Sinonereis heteropoda and Nicon sinica are deposited in the collections of the Marine Biological Museum, Chinese Academy of Sciences (MBMCAS). Specimens were examined using a Zeiss Stemi SV 11 Apo stereomicroscope; to observe parapodial features and chaetae, some parapodia were removed and mounted in semi-permanent slides with ethanol-glycerol to be observed under a Zeiss Axiostar plus compound microscope. All parapodia are in anterior view. Photographs were taken with an AxioCam MRc5 digital camera with an adaptor.

remarks
The original diagnosis by Wu & Sun (1979) focused in the presence of dorsal cirri with 'inflated' cirrophores in anterior chaetigers. Relevant features included in the new diagnosis are the presence of notopodial prechaetal lobes throughout the body, the presence of dorsal lobes in natatory chaetigers, the occurrence of notopodial dorsal ligules from chaetiger 4 in both atokes and epitokes (instead of 3 as usual in most nereidids), and the lack of heteronereid transformation in females. Other key features are the lack of both upper and lower lamellae (usually upper or both lamellae are present) and crenulations in dorsal cirri of natatory chaetigers. Revision of Sinonereis Wu & Sun, 1979 Wu et al. (1985) placed Sinonereis into the subfamily Nereidinae based on the presence of biramous parapodia, a small number of chaetae in the first chaetigers, and single ventral cirrus in all chaetigers (Wu et al. 1985: 44). Later, Sun & Yang (2004) placed Sinonereis in the subfamily Gymnonereidinae sensu Fitzhugh (1987) because of the lack of paragnaths in pharynx, and the presence of biramous parapodia.
In the phylogenetic analysis by Santos et al. (2005), Sinonereis has an uncertain subfamily condition, a similar condition for several other genera. In their cladograms, Sinonereis appeared in a clade together with Leptonereis Kinberg, 1865, Tylonereis Fauvel, 1911and Tylorrhynchus Grube, 1866(Santos et al. 2005. This clade was supported by the character of enlarged notopodial dorsal ligules (in posterior chaetigers) (Santos et al. 2005), which match with Leptonereis, Tylonereis, and Tylorrhynchus, but not with Sinonereis. Sinonereis resembles Tylonereis and Tylorrhynchus by having neuropodial falcigers but separated from them by having basally expanded dorsal cirri, and unilobated neuropodial postchaetal lobes (Santos et al. 2005); additional differences with these genera are the presence of pharyngeal papillae and compound spinigers only in Tylonereis, and lack of both notopodial dorsal ligules and neuropodial ventral ligules in Tylorrhynchus, whereas Sinonereis species have no papillae in pharynx, have both compound falcigers and spinigers, and both notopodial dorsal ligules and neuropodial ventral ligules. Wu & Sun, 1979 (
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).

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.

DISCUSSION
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) (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.  Chamberlin, 1919, Nicon Kinberg, 1865, Rullierinereis Pettibone, 1971and Sinonereis Wu & Sun, 1979. Based on Conde-Vela et al. (2018), Knox (1951), Miura (1990), Pettibone (1971), and Wu et al. (1985.