SESARMIDAE Dana, 1851

Guinot, Danièle, Ng, Ngan Kee & Rodríguez Moreno, Paula A., 2018, Review of grapsoid families for the establishment of a new family for Leptograpsodes Montgomery, 1931, and a new genus of Gecarcinidae H. Milne Edwards, 1837 (Crustacea, Decapoda, Brachyura, Grapsoidea MacLeay, 1838), Zoosystema 40 (26), pp. 547-604 : 578-585

Family SESARMIDAE Dana, 1851

REMARKS

The Sesarmidae , which contains nearly 300 species ( Davie et al. 2015c), is known as a solid monophyletic clade, supported by genetic sequences ( van der Meij & Schubart 2014) and larval morphology ( Cuesta et al. 2006; Shahdadi & Schubart 2017). The massive ecological and morphological speciation should be the result of convergent evolution (Schubart et al. 1998; see also Fratini et al. 2005). According to Schubart et al. (2006), Sesarmoides Serène & Soh, 1970 , now Karstama Davie & Ng, 2007, occupies a basal position within the family. Despite the species richness and ecological diversity (typically inhabitants of soft-sediment littoral habitats like marshes and mangroves, also in freshwater and terrestrial habitats, may be found in bromeliad leaf axils, rock rubble, empty snail shells, caves and mountain streams, thereby showing complete independence from the sea, see Schubart & Koller 2005), the family has not been splitted into subfamilies. The external morphology (e.g. carapace quadrate to quadrangular; suborbital, pterygostomial, subbranchial, subhepatic regions and lateral walls of carapace covered in uniform reticulated network of short, hooked, closely-set setae ( Felgenhauer & Abele 1983: figs 1-4); orbits with lower border as channel running obliquely downwards towards buccal cavern; oblique setose ridge running across merus and ischium of mxp3) is unambiguously different from that of Leptograpsodidae n. fam .

ADDITIONAL CHARACTERS

Sternal and male genital features are added, based on a limited number of selected genera.Proepistome usually very developed, transwerse, broad, variously widened ( Abele 1992: fig. 2d; N. K. Ng et al. 2007: fig. 6C; Komai et al. 2004: figs 4C, 5C, 6B, 8B, 9B; Ragioneri et al. 2012: figs 1, 7d); epistome as complex structure, with Vervey’s groove in which the water from the exhalent openings flows towards antenna and orbit, emptying a thin stream over the reticulate network of setae ( Hagen 1978: fig. 2; Abele 1992; Felgenhauer & Abele 1983: fig. 1; Reimer et al. 1998: fig. 2f). Thoracic sternum variously widened, strongly restricted at P1 level. Sternites 1 and 2 separated by suture 1/2. Suture 2/3 well marked, straight or curved, often lined by setae. Sternite 3 completely fused to sternite 4, no suture 3/4, even no lateral trace ( Fig. 10A, B ) ( Davie & Ng 2013: fig. 9). Sternite 8 developed, either exposed medially and with median line or narrowing medially and without median line. Median line extending on sternite 7 (e.g. Sesarma reticulatum , Chiromantes dehaani ), even on sternite 5. (e.g. Neosarmatium meinerti ). Male sternal gonopore ( Fig. 10C ) located posterior to suture 7/8, adjacent to variously expanded episternite 7, shortly separated from P5 coxa ( Guinot 1979 a: fig. 52D; N. K. Ng et al. 2007: fig. 4B; Schubart et al. 2009: 4; see also Karasawa & Kato 2001: fig. 2.20). Penis rather long, well developed, generally basally calcified, may be foliaceous, showing as longitudinal, oblique or horizontal tube variously oriented; may show as seemingly lying in small depression excavated at base of G1 endopodite ( Guinot et al. 2013: fig. 35: Metasesarma aubryi (A. Milne-Edwards, 1869)) .

Karstama ultrapes (previously in Sesarmoides ) is a remarkable exception. It shows a triangular proepistome, which is wedged between two frontal projections, and a widened thoracic sternum. The male gonopore, in contact with the P5 coxosternal condyle, and the penis, resting in a depression of the developed sternite 8 ( Ng et al. 1994: fig. 8B, as Sesarmoides ), also represent an unusual dispositon.

The pleonal locking mechanism, of press-button type, is various in Sesarmidae : occasionally functional at any (moulting stage) size of the individuals, or present but disappearing at a particular moult (button becoming smaller or obsolete, with increasing body size), or absent ( Guinot & Bouchard 1998). A recent study of species of Parasesarma De Man, 1895 and Perisesarma De Man, 1895 has shown that a button is either absent or indistinct, or developed ( Shahdadi & Schubart 2017: fig. 7).

MOLECULAR ANALYSIS

Chiromantes neglectum (De Man, 1895) was found “within an intermingled ‘ Grapsoidea & Ocypodoidea’ clade” ( Xing et al. 2016: 461, fig. 1). Study of complete mitochondrial genome by Xin et al. (2107b) indicated that Sesarmidae , Xenograpsidae and Varunidae have close relationships.

Given all the differences in many respects, it is easy to distinguish Leptograpsidae n. fam. from the Sesarmidae .

Family VARUNIDAE H. Milne Edwards, 1853

REMARKS

Guinot (1978, 1979) implied that the systematic status of the Varuninae must be raised to a full family. The delimitation of the family has been subsequently supported by congruent larval and adult morphology and by molecular studies (Sternberg & Cumberlidge 1998; Cuesta 1999; Schubart et al. 2000b; N. K. Ng et al. 2007). Five subfamilies were recognised by Ng et al. (2008): the nominotypical Varuninae H. Milne Edwards, 1853 , Asthenognathinae Stimpson, 1858 , Cyclograpsinae H. Milne Edwards, 1853 (as Cyclograpsacea), Gaeticinae Davie & N. K. Ng, 2007 , and Thalassograpsinae Davie & N. K. Ng, 2007 . In contrast, according to Števčić (2005) the Varuninae and Cyclograpsinae were grapsid subfamilies, besides the Grapsinae , Gecarcininae and Sesarminae . Later, Števčić (2013), recognising a family level to Gecarcinidae , added two varunine tribes, one grapsid subfamily Gaeticinae Davie & N. K. Ng, 2007 , and elevated Asthenognathinae to family level, with two subfamilies Asthenognathinae and Aphanodactylinae Ahyong & Ng, 2009. Based on a morphology-based cladistic analysis, Karasawa & Kato (2001) suggested the monophyly of Varuninae and Cyclograpsinae under Grapsidae . Varunids are known since the Miocene ( Karasawa 2018).

According to genetic sequences ( Kitaura et al. 2002, 2010; Schubart et al. 2002, 2006; N. K. Ng et al. 2007; van der Meij & Schubart 2014; Tang et al. 2017), the Varunidae is paraphyletic and its current subfamilies are not monophyletic. In view of the traditional morphology, the subfamilial divisions remain confuse, and it is probable that not only the subfamilies (at least some of them) are paraphyletic but, in addition, certain genera or species are at risk of standing clearly outside the major varunid grouping and must be excluded to recover the monophyletic status of the Varunidae . For example, Kitaura et al. (2002) have shown a sister-group relationship between varunine species and Macrophthalmus Desmarest, 1823 , which revealed distinct from studied ocypodid genera (see also Barnes 2010); similarly, van der Meij & Schubart (2014) and Tsang et al. (2014) recovered strong support for a Varunidae + Macrophthalmidae Dana, 1851 relationship. According to Tsang et al. (2018) the Aphanodactylidae Ahyong & Ng, 2009 , considered a monophyletic family, is more closely related to Macrophthalmidae and Varunidae than to Pinnotheridae De Haan, 1833 . The high diversity of mating strategies described by Brockerhoff & McLay (2005) concerns various varunids, instead of grapsids.

The diversity of morphological characters exhibited by the Varunidae demonstrates how a coherent diagnosis of the family is difficult and does not support its monophyly.

The varunid subfamilies Cyclograpsinae H. Milne Edwards, 1837 , Gaeticinae Davie & N. K. Ng, 2007 , Thalassograpsinae Davie & N. K. Ng, 2007 , Varuninae H. Milne Edwards, 1853 cannot accommodate Leptograpsodes (see N. K. Ng 2006: table 1 and key p. 41; N. K. Ng et al. 2007; Davie et al. 2015c: 71). In only one subfamily, the Cyclograpsinae H. Milne Edwards, 1837 , a few representatives of Cyclograpsus H. Milne Edwards, 1837 share some similarities with Leptograpsodiae n. fam. (see below, Cyclograpsinae ).

Asthenognathinae , previously within the polyphyletic family Pinnotheridae , was transferred to Varunidae by Cuesta et al. (2005) based on molecular results. It was raised to separate familial status by Števčić (2005) within the Grapsoidea . Thus, members of Asthenognathinae (type genus: Asthenognathus Stimpson, 1858 ) were moved from Pinnotheroidea to Varunidae in their own subfamily Asthenognathinae (see Števčić 2005; Ng et al. 2008: 226; Davie et al. 2015b, c) or its own family Asthenognathidae Stimpson, 1858 (Cuesta et al. 2005; see also Palacios-Theil et al. 2009; Guinot et al. 2013: table 7). Asthenognathinae was recently found to be nested within Varunidae instead of aligning with pinnotherids ( Tsang et al. 2018). Given the numerous differences, a comparison with Leptograpsodidae n. fam . is superfluous.

Subfamily CYCLOGRAPSINAE H. Milne Edwards, 1837

POSITION OF CYCLOGRAPSUS

Guinot(1979: 209) was the first to recognise that the sesarmines including Cyclograpsus and allied genera showed the same sternal male gonopore structure as varunines (see also Guinot & Bouchard 1998). Ng et al. (2001: 41, 44) included Cyclograpsus into Varuninae but did not recognise the Cyclograpsinae as a separate taxon, similarly to Schubart et al. (2000b). Karasawa & Kato (2001) and Davie (2002: 207) are credited for resurrecting the subfamily Cyclograpsinae H. Milne Edwards, 1853 (=Cyclograpsacea H. Milne Edwards, 1853, long treated as synonymous with Sesarminae Dana, 1851 ), although they took however the conservative approach of treating the Grapsinae , Sesarminae , Cyclograpsinae and Varuninae as grapsid subfamilies (see also Davie & Xuan 2003; Sakai et al. 2006). In the revision of Varuninae by N. K. Ng (2006: 26, 39, 54, 469), which included 16 species of Cyclograpsus , L. octodentatus was not studied. Larval studies and, chiefly, molecular phylogenetic researches, as those of Schubart & Cuesta (1998), Schubart et al. (2000b, 2002: 39, figs 7, 8, table 1), Kitaura et al. (2002), supported close relationship of Cyclograpsus to the Varunidae or Varuninae . Today, Cyclograpsinae is accepted as a distinct clade within the Varunidae (N. K. Ng 2006: 11, 36, 469, 476, 478; N. K. Ng et al. 2007: 234; Ng et al. 2008: 226; Davie et al. 2015a: 41, 2015c: 1120).

So varied is the subfamily Cyclograpsinae that it is difficult to make general statements. Cyclograpsus seems to be the closest member to Leptograpsodes , thus our study will first focus on this genus. As Cyclograpsus , a genus that probably exceeds 20 worldwide distributed species (Davie & N. K. Ng 2007; Ng et al. 2008; Naruse & N. K. Ng 2012; Naruse 2015), is probably not monophyletic, we will restrict our study to the type species C. punctatus (by subsequent designation of Rathbun 1918: 328) and only its allies. They show a small orbit, a real infraorbital margin lacks, and a variously ornamented (granules, tubercles, elongated structures) suborbital crest is present. In cyclograpsines, the strongly developed and suborbital crest can be stridulatory in conjunction with cheliped merus, which is either only thickened and without a differentiated structure, or bears a horny ridge, usually sexually dimorphic ( Tesch 1918; Guinot-Dumortier & Dumortier 1960; Sakai et al. 2006; Davie et al. 2015a). See Stridulatory structures in grapsoids.

The biology of Cyclograpsus punctatus , a species restricted to southern Africa (see Rathbun 1918; Barnard 1950; Garth 1957; Griffin 1968; Fagetti & Campodonico 1971; Emmerson 2016), provides some similarities with that Leptograpsodes octodentatus : it develops aerial respiratory adaptations, so is highly resistant to desiccation, lives semi-terrestrially, enters estuaries and diggs more or less elaborate burrows in the muddy banks of the rivers ( Broekhuysen 1941; Alexander & Ewer 1969: fig. 3b; Emmerson 2016). Leptograpsodes octodentatus lacks the fine reticulated pattern of short curved setae that entirely covers the pterygostome and results in a fine film of water over the setae, characteristic of Cyclograpsus punctatus and sesarmids ( Alexander & Ewer 1969: fig. 4).

COMPARISON OF C. PUNCTATUS AND LEPTOGRAPSODES

The comparaison between Leptograpsodes octodentatus (especially when small specimens are examined, see Fig. 2 A-C) and Cyclograpsus punctatus , which is a relatively small species, reveals a lot of distinguishing characters. Leptograpsodes differs from C. punctatus by, e.g. carapace margin strongly convex and with three weak teeth (only slightly convex, almost straight, with margin subcristate, entire or indistinctly notched in C. punctatus ); anterolateral margin normal (carinate and ventrally hollowed in C. punctatus ); presence of several postero-lateral striae (at most 2-3 faint ridges obliquely connecting to posterolateral margin in Cyclograpsus ); two pairs of frontal lobes (absent in C. punctatus ); carapace dorsal surface grooved (flat and smooth in C. punctatus ); developed suborbital tooth (absent in Cyclograpsus ); sunken, faint, finely granulose suborbital margin, continuous to near inner limit of orbit and paralleled by developed stridulatory suborbital crest (a thickening encircling and surrounding base of eyestalk in middle of orbit, eclipsed by prominent suborbital crest having a stridulatory role in C. punctatus ); shape of epistome; mxp3 merus without oblique setose crest (with oblique setose crest in C. punctatus ); pterygostome with shallow, simple vertical groove, parallel to buccal cavity (without vertical groove in C. punctatus ); subhepatic, pterygostomial and subbranchial regions covered by pubescence lacking reticulate pattern (reticulated network of short hooked setae in C. punctatus ).

The shape of the orbit, with a stridulating suborbital crest in both genera, merits careful comparison: a close scrutiny reveals their discrepancy. In Cyclograpsus punctatus the orbit is small and closed laterally, a real infraorbital margin lacks and there is only a strongly developed, coarsely granulated suborbital crest that acts in conjunction with variously thickened inner margin of cheliped merus. In Leptograpsodes the large orbit is opened laterally, there is a faint but very distinct suborbital margin, with, in addition, subparallel to and below, a suborbital crest consisting of numerous, very fine and regular granules; this crest (pars stridens) is stridulatory in conjunction with a smooth, delimited crest (plectrum) at inner face of cheliped merus.

The status of all other Cyclograpsus is uncertain. That Cyclograpsus is not monophyletic was shown by the specific disparity of larval features ( Gore & Scotto 1982; Cuesta & Rodríguez 1994) and of locking-pleonal mechanism ( Guinot & Bouchard 1998; Köhnk et al. 2017). As a result, all species assigned to Cyclograpsinae need a reevalution, as Naruse & N. K. Ng (2012) has done for Cyclograpsus lophopus Nobili, 1905 that revealed to be a sesarmid and became Cyclorma lophopus (Nobili, 1905) . C. granulosus H. Milne Edwards, 1853 , a conspicuous species occurring on rocky shorelines in southeastern Australia including Tasmania ( Campbell & Griffin 1966; Griffin 1971), and known by its completely sequenced mitochondrial genome ( Tan et al. 2016), is morphologically quite distinct from Leptograpsodes octodentatus .

The junction of the proepistome to the front is rather similar in the two genera. In Leptograpsodes sternal suture 1/2 strongly marked, sternites 1 +2 semi-ovate; suture 2/3 straight (in C. punctatus sternite 1 individualised, with thick ridge at the location of suture 1/2, see Fig. 9A, B ); in Leptograpsodes sternite 8 only developed laterally, a minute portion visible posteriorly when pleon is folded ( Fig. 3C ) (in C. punctatus sternite 8 developed, medially exposed, and with large portion visible dorsally when pleon is folded); in Leptograpsodes male gonopore close to P5 coxa and far from suture 7/8; penis long, emerging on sternite 8, not very far from suture 7/8, see Fig. 3B ) (in C. punctatus male gonopore far from P5 coxa; penis short, see Fig. 9C ).

OTHER GENERA OF CYCLOGRAPSINAE

The status of all other genera included in Cyclograpsinae , e.g. Helograpsus Campbell & Griffin, 1966 , Metaplax H. Milne Edwards, 1852 (see Karasawa & Kato 2001: fig. 2.24; Davie &

Xuan 2003), Paragrapsus H. Milne Edwards, 1853 (e.g. with P. laevis ( Dana, 1851) , the “mottled shore crab” from Southeastern Australia), deserves a thorough examination.

Subfamily GAETICINAE Davie & N. K. Ng, 2007

INCLUDED GENERA. — The subfamily consits of only a few genera, notably Gaetice Gistel, 1848 , type genus (type species Gaetice depressus (De Haan, 1833)) , Acmaeopleura Stimpson, 1858 , Gopkittisak Naruse & Clark, 2009 , Pseudopinnixa Ortmann, 1894 , Proexotelson Naruse, 2015 ; Sestrostoma Davie & N. K. Ng, 2007 (see Davie & N. K. Ng 2007; Komai & Konishi 2012; Naruse 2015).

REMARKS

This subfamily is remarkable for having mouthparts and thoracic sternum highly modified for suspension feeding, and male pleonal somites 3-6 functionally fused. In gaeticines (see Davie & N. K. Ng 2007: figs 5H, 7B, Gaetice depressus ; Komai & Konishi 2012: fig. 2D, E, Pseudopinnixa carinata Ortmann, 1894 ; Naruse 2015: fig. 1a-d: Gaetice depressus , Sestrostoma balssi (Shen, 1932) , S. depressum (Sakai, 1965) , Acmaeopleura parvula Stimpson, 1858 , respectively), the first sternites are peculiar, being medially hollowed to receive the setal brush of mxp3 palp. Sternite 1 is triangular; sternite 2 is distinctly produced anterolaterally and easily recognisable; the well marked suture 2/3 encompasses diverse patterns (Davie & N. K. Ng 2007: 216), in particular in Proexotelson , in which the long sterno-pleonal cavity (together with long pleon, long G1) completely covers the sternal plate and joins the buccal cavity ( Naruse 2015: figs 6B, 8).

In the type genus and species Gaetice depressus ( Fig. 9 D-F) the first sternites are highly modified as precedingly indicated, which makes difficult interpretation of sutures. A suture 2/3 is clearly visible; sternites 1 and 2 are fused, the line of setae that crosses not seemingly being a true suture; sternite 8 is broad, developed medially, and with a median line (not clearly visible in the figure of Davie & N. K. Ng 2007: fig. 5H); the exposed lateral portion is transversally crossed by a deep, complete sulcus that joins the gonopore to the P5 coxo-sternal condyle. A large portion of sternite 8 is exposed laterally when pleon is folded. The median line extends on sternite 8 and 7. The male sternal gonopore ( Guinot 1979: fig. 52G; Davie & N. K. Ng 2007: fig. 5H) is far from P5 coxa and from suture 7/8. The penis of Gaetice resembles that of Varuna and seems to be able to be applied against the gonopore (as in Varuna , see Guinot et al. 2013: fig. 36).

Naruse & Clark (2009: 66, fig. 2b) described the male gonopore of Gopkittisak as “appearing from distal end of thoracic sternite 8” ( Guinot et al. 2013: 144 erroneously accepted this interpretation): the suture that is figured between the gonopore and the P5 coxa does not denote the suture 7/8 but, instead, probably represents the complete sulcus above-mentioned; the visible sternite only corresponds to sternite 8 crossed by this sulcus (instead of sternites 7 and 8 as in the caption). Acording to Ng (2012: fig. 5B), in Brankocleistostoma Števčić, 2011 the very short sternites 1 and 2 are completely fused, being separated from the longitudinally narrow sternite 3 by a rim: we do not agree with this interpretation, the distinct suture supposedly separating sternites 3 and 4 actually should correspond to suture 2/3. In Gopkittisak , in which anterior sternites are only slightly concave to accommodate setae of mxp3 palp, Komai (2011: fig. 2F) described that thoracic sternites 1-3 were fused, a transverse rim being the bordering of sternite 4.

The differences between Gaeticinae and Leptograpsodidae n. fam . are so numerous that a comparison is not warranted.

Sufamily HELICEINAE Sakai, Türkay & Yang, 2006

INCLUDED GENERA. — Helice De Haan, 1833 (type genus); Helicana K. Sakai & Yatsuzuka, 1980 ; Neohelice Sakai, Türkay & Yang, 2006 ; Chasmagnathus De Haan, 1833 .

REMARKS

Heliceinae , replacement name for Helicinae Kossmann, 1877 (considered a nomen oblitum), is here recognised. A diagnosis of the subfamily lacks since Kossmann (1877: 57) established the taxon only in a key, whereas Sakai et al. (2006: 2, 7) did not formally provide one in their study of the “ Helice / Chasmagnathus complex ”, only listing the characters shared by the two genera. Austrohelice Sakai, Türkay & Yang, 2006 and Pseudohelice Sakai, Türkay & Yang, 2006 are not included for now, waiting for further investigations.

DIAGNOSIS

Carapace subquadrate, lateral margins varying from subparallel to strongly convergent, usually armed with two epibranchial teeth behind exorbital tooth. Front much narrower than half exorbital width; exorbital width not markedly exceeding carapace length. Orbit long, not closed laterally. Eyestalks not nearly as broad as front. Proepistome as wide triangular or pentagonal plate, its very narrow tip inserted under front ( Tavares 1989: fig. 21, as Chasmagnathus granulatus Dana 1851 , now Neohelice granulata ). Stridulatory apparatus usually present (e.g. Helice , Helicana , Chasmagnathus ): pars stridens formed by suborbital ridge composed of granules or tubercules, sexually dimorphic (ridge often heteromorphic in males), rubbed by prominent horny ridge on inner margin of cheliped merus; may be absent. Reticulation on pterygostomial regions poorly developed. Thoracic sternum wide; sternite 1 separated from sternite 2 by convex ridge; suture 2/3 straight; sternite 8 developed, exposed medially, not deeply notched by posterior emargination. Deep median line usually extending from sternite 8 to sternites 6 and even 5, but intermittently. Male gonopore in posteriormost location in relation to suture 7/8. G1 with suture of sperm channel usually torsioned towards dorsal face, except in Chasmagnathus .

REMARKS

The wide thoracic sternum ( Fig. 9G, H ) is typical in having a deep median line intermittently extending from sternite 8 to sternites 5 or at least 6, this corresponding to a variously developed and high median plate (see Sakai et al. 2006: figs 1, 2, 14, 15, 23; note that on their fig. 1 “Mp” corresponds to the median line). The thoracic sternite 1 is triangular; suture 1/2 is strong, convex; sternite 3 is completely fused to sternite 4 as in all Grapsoidea (on fig. 1 of Sakai et al. 2006, “III” actually corresponds to sternite 2): both fused sternites 3 and 4 are separated from sternite 2 by a conspicuous suture (suture 2/3) as shown by N. K. Ng et al. (2018: 6, fig. 1B); when pleon is folded, sternite 8 is exposed, widely ( Helice ) or narrowly ( Chasmagnathus ). The male gonopore ( Fig. 9I ) emerges in middle of sternite 8, far from P5 coxa and from suture 7/8; in Helice (see Guinot 1979: fig. 52I; Sakai et al. 2006: figs 1, 14), Helicana ( Sakai et al. 2006: figs 14, 35) and Neohelice ( Sakai et al. 2006: fig. 92), a conspicuous complete sulcus joins the gonopore to the P5 coxo-sternal condyle; it is incomplete in Chasmagnathus (see Sakai et al. 2006: fig. 7). The opercular cover of the vulva in Helice and Chasmagnathus shows a correspondence between the direction and torsion of the G1 and the shape of the vaginal aperture ( Sakai et al. 2006: 6; see also Shih & Suzuki 2008; Guinot et al. 2013: 36).

The stridulatory apparatus (Guinot-Dumortier & Dumortier 1960: fig. 5b, f), well documented by Sakai et al. (2006: figs 3, 10c, 17, 38-40, 57, 58, 60-66, table 3), is present in most members of the subfamily; the species in which the plectrum lacks in both sexes do not stridulate. Shih & Suzuki (2008) criticised the key morphological characters used by Sakai et al. (2006) and, in particular, their variations within species and between sexes.

The poorly known and probably paraphyletic Pseudohelice is for the moment not included in the subfamily because of its sternal features: median line and median septum only developed on sternite 7 and very small or absent on sternites 5 and 6 ( Sakai et al. 2006: figs 2, 51); male gonopore indicated as close to sternal suture 7/8 ( Sakai et al. 2006: fig. 50); G1 with or without torsion; absence of stridulatory plectrum, at least in some members. Austrohelice is not included for the same reasons: median line and septum not developed; faint sulcus on sternite 8 ( Sakai et al. 2006: figs 2, 86, 87); no plectrum.

Genetic studies including Helice and allied genera are related to their intrarelationships (e.g. Shih & Suzuki 2008; Yin et al. 2009; Zang et al. 2009; Ituarte et al. 2012; Xu et al. 2012) or interrelationships ( Kitaura et al. 2002; Schubart et al. 2006; Xu 2010; Xin et al. 2017a; Tang et al. 2018).

Subfamily THALASSOGRAPSINAE Davie & N. K. Ng, 2007

INCLUDED GENERA. — The subfamily is monotypic, with its type genus Thalassograpsus Tweedie, 1950 with a single species, Thalassograpsus harpax (Hilgendorf, 1892) , that lives under coral stones or rocks in sheltered rocky shores ( Davie 2002; Bouchard et al. 2013; Naderloo 2017).

REMARKS

Davie & N. K. Ng (2007) have listed the unique apomorphies of the subfamily, e.g. frontal margin with short distinct lateral sulcus just posterior to lateral frontal margin, and separated from inner orbital margin (in other Varunidae frontal margin continuous with orbital margin); mxp3 not gaping when closed (more or less gaping in Varuninae , Cyclograpsinae and Gaeticinae ); mxp3 merus and ischium lacking visible longitudinal sulcus (distinctly visible in other varunine subfamilies); male pleon with segments 5 et 6 functionally fused, but sutures visible. The assertion of Davie & N. K. Ng (2007: 262) that the medial groove is proportionately wide on sternites 8 and 7 (other subfamilies with narrower medial groove in sternite 8) in our opinion corresponds in Thalassograpsus to the much more developed sternite 8 (thus more dorsally visible than in Cyclograpsus ) and to a suture 7/8 as long as preceding sutures and reaching the bottom of the sterno-pleonal cavity, thus much more longer than in Cyclograpsus . We agree with the first part of the sentence of Davie & N. K. Ng (2007: 258) “suture of thoracic sternite 3/4 not visible” but not with the second term of the alternative, “slightly visible in all other subfamilies”: the suture 3/4 lacks, as in all Grapsoidea .

Other characters of the subfamily are: sternites 1 and 2 fused (no suture 1/2), sternite 1 narrow and distinctly tapering at tip; suture 2/3 present but thin ( Fig. 9 J-K); suture 3/4 absent; sutures 4/5-7/8 interrupted; sternite 8 developed; median line visible on long portion of sternite 8 and extending on sternite 7 ( Fig. 9K, L ); episternites 5 and 6 very narrow and long; male gonopore in middle of sternite 8, far from suture 7/8 and from P5 coxa, a large part of sternite 8 being intercalated between gonopore and P5 coxo-sternal condyle; proepistome not forming developed structure ( Bouchard et al. 2013: fig. 26B, D); stridulatory apparatus: suborbital crest separated in at least three portions (pars stridens) rubbing against marked thickening (plectrum) on inner edge of cheliped merus ( Fig. 11B, C ) ( Tweedie 1954; Davie & N. K. Ng 2007); press-button mechanism typical.

COMPARISON WITH LEPTOGRAPSODIDAE N. FAM Leptograpsodidae n. fam . shares with Thalassograpsinae the presence of a stridulatory apparatus, however different. In Leptograpsodes suborbital crest is composed of homomorphic granules and the plectrum is a delimited ridge on P1 merus ( Figs 1G ; 2C, D ; 3D ); in Thalassograpsus harpax the suborbital crest consists of heteromorphic tubercles and the plectrum is only a thickening on P1 merus, see Fig. 11B, C ).

Subfamily VARUNINAE H. Milne Edwards, 1853

INCLUDED GENERA. —The Varuninae includes a large number of genera. Main features of Varuninae are provided by N. K. Ng (2006: 37 and table 1, 2007) and Davie et al. (2015c: 1119).

COMPARISON WITH LEPTOGRAPSODIDAE N. FAM

The traditional characters that may be used to differentiate Leptograpsodidae n. fam . from Varuninae could be, e.g. carapace rounded, with very convex margins in Leptograpsodidae n. fam . (in Varuninae varying from quadrate to quadrangular, lateral margins varying from subparallel to moderately convex); front about half width of carapace (vs less than half maximum carapace width); two pairs of postfrontal lobes (vs without four postfrontal lobes); pterygostome, subbranchial, subhepatic regions setose (vs glabrous); suborbital crest stridulatory (vs not stridulatory); mxp3 largely gaping when closed, with antero-external angle of merus not produced, (vs small, rhomboidal gape; antero-external angle of merus strongly produced and auriculate).

For the sternal and male genital features, we will focus our comparison to the type genus Varuna H. Milne Edwards, 1830 and its type species V. litterata . In all examined varunines: male gonopore far from P5 coxa and from suture 7/8, but distance between the genital orifice and suture 7/8 varying among genera. In V. litterata thoracic sternum characterised by: sternite 1 triangular; sternites 1 + 2 separated from sternite 3 by suture; sternite 4 weakly restricted at level of chelipeds; episternites 4-6 elongated and narrow ( Fig. 9M, N ); episternite 7 practically joining P5 coxo-sternal condyle; sternite 8 developed medially, not deeply notched by narrow posterior emargination, and largely exposed when pleon is folded; conspicuous rim on sterno-pleonal cavity at level of telson; marked, deep, long median line on sternites 8, 7 and 6 ( Fig. 9N, O ); typical press-button and persistent throughout the life in males, with socket slightly remote from pleonal margin ( Guinot & Bouchard 1998: fig. 23A). Male gonopore, located far from P5 coxa, opening on vertical slope of sterno-pleonal cavity; P5 coxo-sternal condyle prolonged by incomplete sulcus. Penis, directed obliquely, showing calcified basal portion and well-developed, foliaceous papilla that may clearly invaginate inside gonopore, with calcified portion acting as operculum ( Fig. 9O ) ( Guinot 1979: fig. 52H, pI. 20, fig. 5; N. K. Ng et al. 2007: fig. 4E; Guinot et al. 2013: fig. 36).

For the genital disposition of species of Eriochei r De Haan, 1835 and allies, see Bouvier 1940: fig. 186B; Guinot 1979: fig. 53F; Guinot & Bouchard 1998: fig. 23B; N. K. Ng et al. 1999: figs 2Ci, 2Cii, 4A. In fresh material of Platyeriocheir formosa there is evidence of an invagination of the penis, at least of the papilla, the calcified basal portion of the penis acting as an operculum.

The median line extends along sternites 8- 6 in Neoeriocheir leptognathus (Rathbun, 1913) as shown by N. K. Ng et al. (1999: figs 2Ci), likewise in Varuna , but only on sternites 8 and 7 in Eriocheir sinensis and Platyeriocheir formosa , see N. K. Ng et al. (1999: figs 2Cii, 4A, respectively). Such divergences are not necessarily valid indices to assess generic or even subfamilial status, but a new morphological examination is needed. For other genera, see data in Guinot et al. 2013: 143.

MOLECULAR ANALYSIS

The complete mitochondrial genome is known for some species of Varuna ( Lin et al. 2018) and Eriocheir ( Tang et al. 2003; Liu et al. 2015; Li et al. 2016; Wang et al. 2016; Xin et al. 2017b). Assignation of Eriocheir to the Varuninae by Balss (1957) and Guinot (1979), to Varunidae Schubart et al. (2000b) in a molecular study, and by Clark (2006). Analysis of the nucleotide sequences of the 13 mitochondrial proteincoding genes showed that Eriocheir sinensis , E. hepuensis Dai, 1991 , E. japonica , and Helice latimera Parisi, 1918 clustered together with high statistical support, these species having a sister-group relationship ( Xin et al. 2017b, as Eriocheir japonica sinensis , E. japonica hepuensis and E. japonica japonica , respectively). The molecular data of Chu et al. (2003: table 2) had previouly shown substantial divergences between species of Eriocheir sensu lato and Varuna litterata , and led to the conclusion that the five “mitten crab” species, always clustering together, constituted a monophyletic group genetically distinct from V. litterata . The unstable state of the Varuninae accepted as including Eriocheir and Varuna was confirmed. A new reappraisal based on reliable morphological characters will probably lead to some changes in the systematics of the subfamily.

Family XENOGRAPSIDAE N. K Ng, Davie, Schubart & Ng, 2007

INCLUDED GENERA. — Xenograpsus Takeda & Kurata, 1977 .

REMARKS

The unusual genus Xenograpsus ( Takeda & Kurata 1977) , originally assigned to the Varuninae , shares some morphological characters with other grapsoid families, but evidence from adult and larval morphology ( Jeng et al. 2004a) has shown that it should be regarded as belonging to a separate family. Family Xenograpsidae , established by N. K. Ng et al. (2007), only includes three Xenograpsus species all associated with shallow hydrothermal vents: X. novaeinsularis Takeda & Kurata, 1977 (type species) from the Ogasawara Islands and the Marianas Arc; X. testudinatus Ng, Huang & Ho, 2000 from the Taiwan Arc and Japan (N. K. Ng et al. 2014: in the title of that paper the family is erroneously referred to Grapsidae , owing to a lapsus muris); and X. ngatama McLay, 2007 from Brothers Mount in New Zealand. They are the only grapsoids that live in such a harsh environment ( Jeng et al. 2004b; N. K. Ng et al. 2014; Hu et al. 2016).

The absence of gap between the quadrate mxp3 (vs a rhomboidal gap in Leptograpsodes ), considered a diagnostic character of the family Xenograpsidae by N. K. Ng et al. (2007: 250) and considered unique amongst the Grapsoidea , is in fact a character also shared by Glyptograpsidae (see Schubart et al. 2002: fig. 1; N. K. Ng et al. 2007: fig. 7G), Plagusiidae , and various varunid genera of the subfamily Gaeticinae that show a characteristic structure of mxp3 related to suspension feeding (Davie & N. K. Ng 2007; Naruse 2015: table 2).

MOLECULAR ANALYSIS

Genetic sequences by Schubart (2011), with Varuna litterata as outgroup, and by Ip et al. (2015) indicate a close relationship of Leptograpsodes to Xenograpsidae , even a possible sister-taxon relationship with Xenograpsu s. The question is therefore to test whether the xenograpsid morphology provides the accurate traits to corroborate the DNA data or whether there is another case of incongruence between the currently adopted classification and molecular phylogenetics. Xenograpsus testudinatus was shown to have distinct gene order ( Ki et al. 2009). According to the gene order analysis of brachyuran mitochondrial genomes by Basso et al. (2017), in which Brachyura appears to be a hot-spot of gene order diversity within the phylum Arthropoda, XenGO is an apomorphy currently known only for X. testudinatus . According to Wang et al. (2018b: 39, fig. 6), based on the complete mitochondrial DNA (mtDNA) sequences, Xenograpsus testudinatus and Sesarmidae was found forming a group with close relationships.

The morphological characters of Xenograpsus testudinatus have been studied and illustrated by N. K. Ng (2006) and N. K. Ng et al. (2007). The comparative characters are: proepistome inserted as thin tongue into lower margin of front (N. K. Ng et al. 2007: figs 3B, 6A) (also thin tip in Leptograpsodes ); orbit almost complete, in the form of deep sunken cavity (N. K. Ng et al. 2007: fig. 5A) (partially opened laterally in Leptograpsodes ); suborbital margin not stridulatory (N. K. Ng et al. 2007: fig. 5G) (suborbital margin with stridulatory function in Leptograpsodes ); mxp3 broad, operculiform, lacking rhomboidal gap (N. K. Ng et al. 2007: fig. 7A) (gaping in Leptograpsodes ); typical pleonal-holding mechanism present: rather big sternal button and deep pleonal socket (as in Leptograpsodes ); G1 strongly calcified, short and stout (long, quite slender, with blunt, horny tip and flap on sternal surface in Leptograpsodes ).

ADDITIONAL STERNAL AND MALE GENITAL CHARACTERS

In Xenograpsidae (our data are only based on X. testudinatus , the only species that we have examined), the thoracic sternum ( Fig. 8M, N ) (N. K. Ng et al. 2007: fig. 3H) shows: complete suture 2/3 and no anterior suture or depression that could be suture 1/2; sutures 4/5-7/8 incomplete, suture 7/8 being shorter; rather wide sternite 8 but, as notched by deep triangular posterior emargination, not exposed medially and only lateral; median line on sternite 7 only (not clearly shown by N. K. Ng et al. 2007: fig. 3H); no traces of bridge. Male gonopore ( Fig. 8O ) (N. K. Ng et al. 2007: fig. 4A) opening on sternite 8 by wide aperture along lateral margin of posteriorly expanded episternite 7; aperture rather far from suture 7/8 but close to P5 coxo-sternal condyle; expanded episternite 7 joining P5 coxo-sternal condyle, extending in direction of sternite 8, thus getting very close to it but without reaching it; penis short, not exposed when pleon is folded.

Concerning the sternal and male genital features, Xenograpsidae and Leptograpsodidae n. fam share: sterno-pleonal cavity very wide; press-button typical; male gonopore not far from P5 coxo-sternal condyle; sternite 8 reduced to its lateral portion due to pronounced posterior emargination reaching sternite 7; median line on sternite 7 only. But they differ by the obvious traditional traits already known and also by: suture 1/2 convex as complete, thickened ridge, and suture 2/3 complete in Leptograpsodidae n. fam . (only suture 2/ 3 in Xenograpsidae , although two anterior sutures are figured for X. testudinatus by N. K. Ng et al. 2000: fig. 3B and by N. K. Ng et al. 2007: fig. 3H); presence of thick sternal bridge in Leptograpsodidae n. fam . (no bridge in Xenograpsidae ); very small portions of penis and sternite 8 dorsally visible in Leptograpsodidae n. fam . (nothing visible in Xenograpsidae ).

The genital condition of Xenograpsus presents some similarities with that of Plagusiidae ( Fig. 8L ) ( Guinot 1979: fig. 52E; N. K. Ng et al. 2007: fig. 4C) where the elongated episternite 7 joins the sternite 8 and separates the gonopore from the P5 coxa.

Figures

FIG. 10. — Sesarmidae: Sesarma reticulatum Say, 1817, ♂ 22.1× 27.0 mm, New Jersey, MNHN-IU-2017-8399 (=MNHN-B25784): A, thoracic sternum (brushed) with pleon; B, thoracic sternum (brushed) without pleon; C, genital region with gonopore and penis. Scale bars: 10 mm.

FIG. 2. — Leptograpsodes octodentatus (H. Milne Edwards, 1837): A-D, neotype, ♂ 17.3× 20.6 mm, Australia, Tasmania, King Island, TMAG G1033: A, dorsal view; B, ventral view; C, frontal view, with suborbital ridge as pars stridens; D, close-up view of plectrum as whitish ridge on P1 merus (see arrow); E, syntype of L. webhaysi Montgomery, 1931, ovigerous ♀ 27.0 ×34.0 mm, Abrolhos, WAM C71736. Scale bars: 10 mm.

FIG. 9. — Pleon, thoracic sternum and genital region of Varunidae: A-C, Cyclograpsinae: Cyclograpsus punctatus H. Milne Edwards, 1837, ♂ 24.9× 30.8.0 mm, South Australia, Kangaroo Island, MNHN-IU-2013-14994 (=MNHN-B12561); D-F, Gaeticinae: Gaetice depressus (De Haan, 1835), ♂ 15.7 × 18.0 mm, China, Amoy,MNHN-IU-2013-14990 (= MNHN-B12089); G-I, Heliceinae Sakai, Türkay & Yang, 2006: Helice tridens (De Haan, 1835), ♂ 28.7 ×34.2 mm, Japan, MNHN- IU-2016-10762 (=MNHN-B12098);J-L,Thalassograpsinae:Thalassograpsus harpax (Hilgendorf,1892),♂ 8.1× 9.3 mm,Scattered Islands,MNHN-IU-2013-16120; M-O, Varuninae: Varuna litterata (Fabricius, 1798), ♂ 49.5 ×57.0 mm, Madagascar, MNHN-IU-2013-14987. Scale bars: A-K, M-O, 10 mm; L, 5 mm.

FIG. 3. — Leptograpsodes octodentatus (H. Milne Edwards, 1837), ♂ 51.8 ×68.3 mm, South Australia, MNHN-IU-2013-14993 (ex NMV J55301-1): A, thoracic sternum (note sternite 8 not developed medially, only exposed laterally); B, genital area with male gonopore and penis; C, posterior part of thoracic sternum with pleon; D, front and orbit. Abbreviations: b, bridge; b.p., press-button; c, coxo-sternal condyle; cx1-5, P1-P5 coxae; e.p., exposed proximal portion of penis; e.t., extraorbital tooth; e4-e7, episternites 4-7; i.b., suborbital border; i.s., incomplete sulcus; i.t., suborbital tooth; m.l., median line; mxp3; third maxilliped; P1, P2, P3, pleonal somites 1-3; p, penis; p.e., posterior emargination; p.p., proximal portion of penis; p.r., pleonal rim; s.c., stridulating crest; s.p., sterno-pleonal cavity; 1-8, thoracic sternites 1-8; 1/2-7/8, thoracic sternal sutures 1/2-7/8. Scale bars: 10 mm.

FIG. 11. — Stridulatory apparatus:A, Discoplax longipes A.Milne-Edwards,1867, ♀ 32.6× 37 mm, Loyalty Islands, Lifou, Inegoj Cave, MNHN-IU-2008-11402 (= MNHN-B24815): plectrum as a ridge on cheliped merus (see arrow); B, C, Thalassograpsus harpax (Hilgendorf, 1892), ♂ 5.3× 5.7 mm, Scattered Islands,MNHN-IU-2013-16120; B, pars stridens consisting of elongated tubercles on suborbital ridge (see arrows);C, plectrum as a thickening (see arrow) on inner edge of cheliped merus. Scale bars: A, 5 mm; B, C, 2 mm.

FIG. 1. — Leptograpsodes octodentatus (H. Milne Edwards, 1837), ♂ 51.8 ×68.3 mm, South Australia, MNHN-IU-2013-14993 (ex NMV J55301-1): A, carapace, dorsal surface; B, chelipeds; C, thoracic sternum with pleon (setal tufts visible); D, thoracic sternum without pleon; E, genital area with male gonopore and penis; F, G1, two views; G, front, orbit, antenna (with articles 1-4 and flagellum) and suborbital ridge as pars stridens. Scale bars: 10 mm.

FIG. 8. — Pleon, thoracic sternum and genital region of Grapsoidea: A, D, G, J, M, thoracic sternum (brushed) with pleon; B, E, H, K, N, thoracic sternum (brushed) without pleon; C, F, I, L, O, genital region with gonopore and penis: A-C, Grapsidae: Grapsus grapsus Lamarck, 1801, ♂ 23.8 ×26.9 mm, Antilles, MNHN-IU-2013-10764 (=MNHN-B24641);D-F, Glyptograpsidae:Glyptograpsus jamaicensis (Benedict,1892),♂ 32.8 ×37.4 mm,Jamaica,MNHN-IU-2017-8401 (= MNHN-B127715); G-I, Percnidae: Percnon planissimum (Herbst, 1804), ♂ 29.7× 27.7 mm, Réunion Island,MNHN-IU-2010-19798 (=MNHN-B24534);J-L, Plagusiidae: Plagusia squamosa (Herbst, 1790), ♂ 43.6 ×46.3 mm, Marquesas Islands, MNHN-IU-2011-8947; M-O, Xenograpsidae: Xenograpsus testudinatus N. K. Ng, Huang & Ho, 2000, ♂ 21.8 ×23.8 mm, NE Coast of Taiwan, MNHN-IU-2013-14995 (= MNHN-B30314). Scale bars: 10 mm.