On the clawed lobsters of the genus Nephropsis Wood-Mason, 1872 recently collected from deep-sea cruises off Taiwan and the South China Sea (Crustacea, Decapoda, Nephropidae)

Abstract Recent deep-sea cruises using Taiwanese research vessels off Taiwan and in the South China Sea yielded seven species of the clawed lobster genus Nephropsis Wood-Mason, 1872. Four species are new records for Taiwan (Nephropsisacanthura Macpherson, 1990, N.holthuisi Macpherson, 1993, N.serrata Macpherson, 1993, and N.suhmi Bate, 1888) and three species are new records of Dongsha (under the jurisdiction of Taiwan) in the South China Sea (N.ensirostris Alcock, 1901, N.stewarti Wood-Mason, 1872, and N.suhmi). Altogether, five and four species of this genus are now known from Taiwan and Dongsha, respectively. The diagnostic characters and coloration are illustrated for most, if not all, of these species.


Introduction
Members of the genus Nephropsis Wood-Mason, 1872 represent the common clawed lobster found in the deep sea world-wide (Macpherson 1990;Holthuis 1991;Chan 1997;Alves-Júnior et al. 2016). At present, 15 species of this genus are recognized (Chan 2010), and with nine of them distributed in the Indo-West Pacific (Macpherson 1990(Macpherson , 1993Griffin and Stoddart 1995;Holthuis 1991;Chan 1997;Watabe and Ii-zuka 1999;Zarenkov 2006). In Taiwanese waters, only one species, Nephropsis stewarti Wood-Mason, 1872, has been formally reported Yu 1988, 1993), and this species can often been caught by commercial deep-sea trawlers although never in large numbers. Recent deep-sea cruises using Taiwanese research vessels off Taiwan and the South China Sea have yielded many species of Nephropsis. Amongst them, N. serrata Macpherson, 1993 had been listed in a molecular phylogenetic study (Tshudy et al. 2009). Close examination of this Nephropsis material reveals seven species, including four new Taiwanese records (N. acanthura Macpherson, 1990, N. holthuisi Macpherson, 1993, N. serrata, and N. suhmi Bate, 1888 and three new records (N. ensirostris Alcock, 1901, N. suhmi, and N. stewarti) around Dongsha (Pratas, under the jurisdiction of Taiwan) in the South China Sea. The present work reports these findings. The two other Indo-West Pacific species those are still not known in Taiwan and adjacent areas are N. carpenteri Wood-Mason, 1885, andN. malhaensis Borradaile, 1910. Both of them appear to be restricted in the Indian Ocean (Macpherson 1990).

Materials and methods
Specimens are deposited in the National Taiwan Ocean University, Keelung (NTOU). The station (stn) designation is preceded by a prefix indicating the actual type of collecting equipment, as follows: Le Drezen type solo hard bottom 12.4 m otter trawl (CD), 4 m French beam trawl (CP), 2.5 m French beam trawl (PCP), and 3 m ORE beam trawl (OCP). Carapace length (cl) is measured along the dorsal midline from the orbital margin to the posterior margin of the carapace. Morphological terminology mainly follows Macpherson (1990). The synonymy provided is restricted to important taxonomic works of the species and previous Taiwanese and South China Sea records.
Abdomen with tergites II-VI bearing conspicuous median carina. Anterior border of pleuron II convex and bearing some spinules, terminating in long, acute point. Anterior border of pleura III-V less convex and also terminating in long, acute point. Strong erect dorsal spine present near base of telson. Uropodal exopod with complete diaeresis.
Carpus of cheliped I with strong anterordorsal spine; outer surface without spine; inner border with a spine somewhat at middle of carpus. Carpus of pereiopod II shorter than palm. Carpus of pereiopod III approximately 2/3 palm length. Dactyli of pereiopods IV and V slightly longer than half propodus length.
Color in life. Body generally reddish with dorsal carapace and abdomen whitish. Eyes whitish.
Remarks. Nephropsis acanthura is reported from Taiwan for the first time. This species and N. occidentalis Faxon, 1893 are the only two species in the genus bearing an erect spine near the base of the telson (Macpherson 1990;Holthuis 1991). The two Taiwanese specimens fit well with the characteristics of N. acanthura in the carapace bearing numerous small granules, the rostrum longer than half carapace length, and the abdominal pleura II-V terminating in a long, acute point (see Macpherson 1990;Holthuis 1991). Nevertheless, there are some variations noticed in the present material compared with those reported by Macpherson (1990). In the Taiwanese specimens, the dactyli of pereiopods IV and V (Fig. 3C) are slightly longer than half propodus length (vs. less than half ). The median groove on the rostrum extends beyond the lateral rostral spines (vs. terminating at the level of lateral rostral spines). The distance between the orbital border and postcervical groove is slightly less (vs. slightly more) than twice the distance between the postcervical groove and posterior border of carapace. Additionally, it is reported that the carapace is less granular in the Indonesian material (Chan 1997). Alcock, 1901 Figs 1C, D, 4 Nephropsis ensirostris Alcock, 1901: 158, pl Diagnosis. Carapace finely granulate. Rostrum more than half carapace length, without lateral spine. Median groove reaching or overreaching midpoint of rostrum. Each subdorsal carina with none or two spines and several granules. Gastric tubercle located closer to orbital border than to postcervical groove. Supraorbital and postsupraorbital spines present. Postcervical groove deep, passing dorsal midline of carapace. Pair of dorsal spines located just behind postcervical groove. Distance between orbital border and postcervical groove less than twice distance between postcervical groove and posterior border of carapace.

Nephropsis ensirostris
Abdominal tergites I-V with conspicuous transverse grooves. Dorsal median carina present on tergites II-VI. Anterior borders of pleura II-V granulated, spineless, terminating in a long, acute point. Anterior border of pleuron II more convex than those of other pleura. Uropodal exopod with distinct but incomplete diaeresis.
Cheliped I with little pubescence; carpus with well-developed anterodorsal spine, outer spine on terminal half and inner spine at about mid-length. Carpus of pereiopod II slightly longer than palm. Carpus of pereiopod III more than half palm length. Dactyli of pereiopods IV and V approximately 2/3 propodus length.
Color in life. Body generally pinkish to whitish, with rostrum, tail fan, and antennal and antennular flagella reddish. Eyes whitish.
Distribution. This species has been reported in the Indian Ocean along Gulf of Aden, Laccadive Sea, Bay of Bengal to Andaman Sea. In the western Pacific it is only known from Indonesia and the Philippines. The present material extends its distribution to near Dongsha in the South China Sea. Bathymetric depth ranges from 315 to 1314 m (Macpherson 1990;Holthuis 1991;Chan 1997;Zarenkov 2006).
Remarks. Nephropsis ensirostris can be readily distinguished from other species of the genus by lacking a lateral spine on the rostrum. The two small specimens collected off west of Dongsha agree well with the description of Macpherson (1990), except for the spines on the subdorsal carina are missing in the male ( Fig. 4B; see also Chan 1997). These spines are present in Macpherson's (1990) material as well as in the female specimen reported here (Figs 1D, 4A). Macpherson, 1993 Figs 1E, F, 5 Nephropsis holthuisi Macpherson, 1993:  Diagnosis. Carapace sparsely granulate. Rostrum 0.6-0.8 times carapace length, with pair of lateral spines. Median groove on rostrum reaching or overreaching lateral rostral spines. Subdorsal carinae with 1-4 spines posterior to supraorbital spines. Supraorbital spine well-developed, followed by distinct post-supraorbital spine. Distance between level of supraorbital spine and gastric tubercle approximately 0.4 times the distance between gastric tubercle and postcervical groove. Postcervical groove passing dorsal midline of carapace. Distance between orbital border and postcervical groove 1.5-1.9 times distance between postcervical groove and posterior border of carapace.

Nephropsis holthuisi
Abdominal tergites II-VI with distinct dorsal median carina. Anterior border of each pleuron spineless, more convex in pleuron II, and terminating in long, sharp point on pleura II-V. Uropodal exopod with complete diaeresis.
Cheliped I sparsely granulate. Carpus shorter than palm, with anterodorsal spine, a spine on inner dorsal border at midlength, and without any accessory spines or granules. Carpus of pereiopod II somewhat shorter than palm. Carpus of pereiopod III 0.6 times palm length. Dactyli of pereiopods IV and V approximately half propodus length.
Color in life. Body generally vermilion red, with dorsal surface of posterior carapace and abdomen pinkish orange. Tips of large chelae and eyes whitish.
Remarks. This species is similar to Nephropsis rosea Bate, 1888 from the West Atlantic. They both have one pair of rostral lateral spines, one pair of post-supraorbital spines, a median carina on tergites II-VI, and a complete diaeresis on uropodal exopods. These two species mainly differ in the position of the gastric tubercle (see Macpherson 1993). The Taiwanese material fits the characteristics of N. holthuisi in the distance between the supraorbital spine and gastric tubercle being less than half (vs. approx. 2/3 in N. rosea) the distance between the gastric tubercle and postcervical groove. Watabe and Iizuka (1999) argued that N. holthuisi can be readily distinguished from N. rosea by the large spine at the midlength of the inner dorsal border of carpus of cheliped I does not have any accessory spines or granules (vs. 1-3 accessory spines in N. rosea). The present specimens also agree in this character.
There are variations in the development of the subdorsal spines in the type series of N. holthuisi from rather granulate in the holotype to distinct in the paratype (Macpherson 1993). The present six specimens from Taiwan all have 1-4 distinct spines on the subdorsal carina (Figs 1F, 5). Watabe and Iizuka (1999) considered such difference as specific and treated the paratype of N. holthuisi as a distinct species N. macphersoni Watabe & Iizuka, 1999. However, all other differences proposed to distinguish N. macphersoni from N. holthuisi by Watabe and Iizuka (1999), such as pereiopods "less pubescent" or "more robust", abdominal tergite "more strongly granulated", are rather vague. Therefore, for the time being N. macphersoni is treated as a synonym of N. holthuisi as already stated by Chan (2010) until more evidence (e.g., from molecular analysis) is available to support that the former is a distinct species. Macpherson, 1993 Figs 2A, B, 6 Nephropsis serrata Macpherson, 1993 Diagnosis. Carapace slightly granulate. Rostrum 0.4-0.8 times carapace length, with pair of lateral spines. Median groove reaching lateral rostral spines. Each subdorsal carinae with 2-6 distinct spines and some granules. Supraorbital spine well-developed, without post-supraorbital spine. Postcervical groove passing midline of carapace. Distance between orbital margin and postcervical groove 1.5-1.9 times distance between postcervical groove and posterior margin of carapace.

Nephropsis serrata
Abdominal tergites smooth, sometimes with some granules on large specimens, without median dorsal carina. Anterior margins of pleura II-V without spines, usually ending in a long, acute point. Uropodal exopod with complete diaeresis.
Cheliped I sparsely granulated, covered with dense hairs. Carpus with anterodorsal spine, 0-1 spine (rarely 0) on inner dorsal border at midlength, and an anteroventral spine on inner margin. Carpus of pereiopod II more or less as long as palm. Carpus of pereiopod III 0.6 times palm length. Dactyli of pereiopods IV and V 0.5-0.6 times propodus length.
Color in life. Body generally whitish with rostrum, distal parts of pereiopods, maxilliped III, antennular and antennal flagella, abdominal pleura, uropods and distal part of telson pinkish red to reddish. Eyes whitish. Eggs greyish yellow.
Remarks. One of the specimens from the lot NTOU M00157 was used and listed in a recent molecular phylogenetic work (Tshudy et al. 2009: table 1), which is the first literature record of this species from Taiwan. Nephropsis serrata is very similar to N. stewarti. They both lack median dorsal carina on the abdomen and mainly differ in the presence or absence of spines on the subdorsal carina (Macpherson 1993). The other distinguishing characters mentioned by Macpherson (1993), such as N. serrata having more elongate lateral rostral spines than supraorbital spines, a slightly shorter rostrum, and a less elongate large chela, are difficult to use (see Macpherson 1993: Figs 7, 8). The Taiwanese specimens all bear distinct spines on the subdorsal carinae and agree well with the original description of the species (Macpherson 1993), except for the carpus of the large cheliped bearing 0-1 (mostly one) rather than two spines on the inner dorsal border at mid-length. Moreover, an ovigerous female (NTOU M02154) is abnormal in having two spines on the right side of the rostrum.
Three recently described species, namely N. hamadai Watabe & Ikeda, 1994, N. lyra Zarenkov, 2006, and N. pseudoserrata Zarenkov, 2006, are treated under the synonyms  of N. serrata by Chan (1997Chan ( , 2010. Some of the differences between N. hamadai and N. serrata proposed by Watabe and Ikeda (1994) have been shown to be inappropriate by Chan (1997). The present Taiwanese material also reflects such an opinion, except for the inner dorsal border of the carpus of the large cheliped always being armed with fewer than two spines at the mid-length (two spines in N serrata by Macpherson 1993 and one spine in N. hamadai by Watabe and Ikeda 1994). In the original description of N. lyra, Zarenkov (2006) argued that this species is closest to N. stewarti and N. grandis Zarenkov 2006. However, N. lyra is actually most similar to N. serrata in bearing 3-4 distinct spines on the subdorsal carina. Since no distinct difference is observed between the original illustrations of N. lyra (Zarenkov 2006: figs 8-11) from N. serrata, and the type localities of both species are from the same area (i.e., off northwestern Australia), these two species are considered as synonyms pending more evidence to support their separation. Another species, N. pseudoserrata described by Zarenkov (2006), based on a single specimen from Sumatra, is also closest to N. serrata in having 1-2 spines on the subdorsal carina. However, Zarenkov (2006) claimed that N. serrata differs from N. pseudoserrata in the subdorsal carina being smooth. As this separation is based on a misinterpretation and the other differences proposed by Zarenkov (2006: table 4) on the armature of the large cheliped are rather variable in this genus, N. pseudoserrata is not recognized as a species distinct from N. serrata.
Abdominal tergites II-V without dorsal median carina. No spines on anterior margin of each pleuron. Anterior margin of pleuron II convex, generally ending in long, sharp point (but rather short and blunt in large specimens). Anterior margins of pleura III-V less convex, each ending in long, sharp point. Uropodal exopod with distinct and complete diaeresis.
Cheliped I densely pubescent. Carpus with anterodorsal and anteroventral spines, and 0-4 dorsal spines on outer margin. Carpus of pereiopod II slightly shorter than palm. Carpus of pereiopod III more than half palm length. Dactyli of pereiopods IV and V approximately half propodus length.
Color in life. Body generally whitish with antennular and antennal flagella, anterior segment of large chelae, dorsal carapace, and abdomen somewhat pale orange. Rostrum, tips of pereiopods II to V, and tail fan pinkish red. Eyes whitish. Pubescence on body light grey and eggs whitish.
Distribution. Widely distributed in the Indo-West Pacific and has been reported from Madagascar, Natal, Mozambique, Kenya, Gulf of Aden, Andaman Sea, Bay of Bengal, Indonesia, Australia, the Philippines, Japan, Taiwan, and now the South China Sea, at depths of 170 to more than 1060 m (Macpherson 1990(Macpherson , 1993Chan 1997;Zarenkov 2006;Poore et al. 2008).
Remarks. The present material collected by Taiwanese research vessels were from the South China Sea; near Dongsha (NTOU M02161, M02170) or the center of the South China Sea (NTOU M02162, M02163).
Color in life. Entire body vermilion red, except tips of large chelae, eyes, most dorsal parts of abdominal tergites I to V, and basal parts of antennular peduncles whitish.
Distribution. Widely distributed in the Indo-West Pacific and recorded from Madagascar, Gulf of Aden, Maldive Sea, Arabian Sea, Indonesia, Australia, New Caledonia, western Tasman Sea, New Zealand, at 786-2029 m deep (Macpherson 1990(Macpherson , 1993Griffin and Stoddart 1995;Poore 2004;Zarenkov 2006;Yaldwyn and Webber 2011). This species is reported for the first time from Taiwan and the South China Sea (including Dongsha).
Remarks. N. suhmi from the Indo-West Pacific and N. agassizii A. Milne-Edwards, 1880 from the West Atlantic (Macpherson 1990;Alves-Júnior et al. 2016) are the only two known species of Nephropsis lacking a diaeresis on uropodal exopods. The present material fits well with the concept of N. suhmi in having the dactylus of pereiopod V approximately half the propodus length (vs. distinctly less than half in N. agassizii;Holthuis 1974: fig. 19;Macpherson 1990: fig. 7c;Alves-Júnior et al. 2016: fig. 1A). The only discrepancy may be that in two (female of NTOU M02134; NTOU M02138) of the present 24 specimens there is a large posterior spine at the base of the pleuron V (Fig. 8C).
Nephropsis meteor Zarenkov, 2006 is closely related to N. suhmi and was described based on a single specimen from the Gulf of Aden (Zarenkov 2006). The characters separating N. meteor from N. suhmi are the merus of large cheliped with two instead of one rows of spines, the postcervical groove dorsally armed with a pair of dorsal spines (vs. no dorsal spines), and the anterior margin of abdominal pleura III-V each bearing two spines instead of one spine (Zarenkov 2006 : table 3). However, in the original description and illustration of N. meteor (Zarenkov 2006: 90, fig. 13B), the anterior margins of pleura IV and V each bearing only one and not two spines as listed in the table of distinguishing characters given by Zarenkov (2006: table 3). In the present material, there are 0-2 distinct spines on the anterior margin of each of the abdominal pleura III-V. The spination on the postcervical groove and merus of large cheliped are also rather variable in the abundant material examined in this study (i.e., 1-2 rows of spines on the merus of the large cheliped and 0-2 distinct spines on the dorsal part of postcervical groove). Thus, N. meteor should be considered as a synonym of N. suhmi as stated by Chan (2010) until there is more evidence to support their separation. Macpherson, 1990 Fig. 9 Nephropsis sulcata Macpherson, 1990: 319, figs 13e-g, 14a, b, 15a, b, 16g  Diagnosis. Carapace generally smooth, with some small granules. Rostrum more than half carapace length, bearing two strong lateral spines. Median groove overreaching distal pair of lateral rostral spines. Posterior portion of subdorsal carina armed with several small spines. Postorbital and post-supraorbital spines present. Postcervical groove crossing midline of carapace. Distance between orbital margin and postercervical groove approximately 1.5 times distance between postcervical groove and posterior margin of carapace.

Nephropsis sulcata
Abdominal tergites II-VI with distinct median carina. Anterior border of pleura II-V convex, each terminating in long, acute point. A single strong spine and 1-3 additional spines on anterior border of pleuron II. Anterior border of pleuron III with two small spines. Posterior border of pleuron V armed with a strong spine. Uropodal exopod with complete diaeresis.
Cheliped I bearing numerous granules on all articles. Carpus with anterodorsal and anteroventral spines; two spines on inner surface; outer surface with one spine on distal half. Carpus of pereiopod III 0.79 times palm length.
Remarks. The present specimen was collected off Dongsha in the South China Sea and the presence of N. sulcata off Dongsha has been reported before (Bruce 1966, as N. atlantica Norman, 1882see Macpherson 1990). Nephropsis sulcata can be distinguished from the closely related Atlantic species N. atlantica by the carpus of the pereiopod II being longer than the palm, and usually bearing a spine on the posterior border of the abdominal pleuron V ( Fig. 9B; see also Chan 1997). Even though both sides of pereiopod II are missing in the present specimen, its remaining part agrees well with the description of N. sulcata by Macpherson (1990).