Raninoidea De Haan, 1839

Van Bakel, Barry W. M., Guinot, Danièle, Artal, Pedro, Fraaije, René H. B. & Jagt, John W. M., 2012, A revision of the Palaeocorystoidea and the phylogeny of raninoidian crabs (Crustacea, Decapoda, Brachyura, Podotremata) 3215, Zootaxa 3215 (1), pp. 1-216 : 70-75

Superfamily Raninoidea De Haan, 1839

Raninoidea De Haan, 1839 : 102.

Type family. Raninidae De Haan, 1839 emend.

Families included. Lyreididae Guinot, 1993 new status, and Raninidae De Haan, 1839 emend.

Diagnosis. Carapace longer than wide, narrow to moderately broad, elongated, urn shaped, fusifom ( lyreidinae ) or ovate, anteriorly broadened or tapering, greatest width varying; moderately convex to roof shaped, may have medial carina ( Notopodinae ). Dorsal surface smooth or variously ornamented, may be scabrous, terraced, eroded, or with particular microstructure; cervical groove generally indistinct or lacking; branchiocardiac grooves usually marked. Anterolateral margins usually with 1‒3 teeth, rarely teeth absent; teeth may be broad, developed, bifurcated or spiniform. Front narrow, generally triangular or subtrapezoidal, may be trifid or replaced by emargination ( Notopodinae ). Orbitofrontal margin varying from narrow to wide; supraorbital margin with 1 or 2 closed or open fissures, may be smooth, lined with granules, spinules or armed with teeth, external tooth usually produced. Orbits well defined, anteriorly or anterolaterally directed; eyestalk short to long, with 1–3 articles, folding when retracted.

Antennules, antennae not located in fossae, positioned behind eyestalks, usually considerably modified. Antennules not folded; antennae usually large, generally with 5 articles, short or long flagellum. Proepistome concealed or well developed; epistome triangular, prominent; endostome large, elongated, strongly excavated, in oxystomian condition. Buccal frame elongated with smooth collar. Mxp3 strongly elongated, narrow, operculiform; endopodite: basis-ischium, merus usually subequal in length; palp small, partially or completely concealed; exopodite weakly extending beyond ischium/merus articulation of endopodite, without flagellum. Mxp1 with exopodite and endopodite expanded, modified, forming exhalant channel; exopodite without flagellum. Pterygostome tumid, with prominent subantennary lobe.

Thoracic sternum narrow posterior to sternite 4, strongly deflected at different levels. Sternite 1 concealed; sternite 2 may be dorsally visible, inclined; sternite 3 usually crown shaped (compressed, ridged in Cyrtorhininae ); sternite 4 usually wide (narrow in Cyrtorhininae ), flat; suture 4/5 variously crescent shaped; sternite 5 laterally expanded; posterior sternites narrow, occasionally linear, may be keeled; sternite 8 variously reduced. Medial line present along posterior sternites, extending to sternite 5 or 6. Sternum/pterygostome junction present, narrow ( Cyrtorhininae , Symethinae ) to wide, rarely absent ( Marylyreidinae n. subfam.). Sternum/exposed pleurites connection variously developed between P1, P2; usually present between P2, P3, may be absent between P2, P3 ( Raninidae , Notopodinae; Marylyreidinae n. subfam.). Posterior part of branchiostegite markedly reduced in height; pleurites 5‒7 partially exposed, calcified (gymnopleurity); exposed pleurites flat or variously excavated, with several protruding outgrowths to attach to branchiostegite. Spermathecal apertures opening anteriorly enclosed by sternite 7; generally close to each other, separated by medial line, recessed in medial depression (‘sunken pit’) (superficial, hooded in Symethinae ). Female gonopores on P3 coxae, male gonopores on P5 coxae.

Sterno-abdominal depression weak; may be incompletely formed, narrow ( Lyreididae ). Abdomen with 6 free somites plus telson; short ( Raninidae ) or long ( Lyreididae ); first somites dorsal, in continuity with carapace; sexual dimorphism not strongly marked. Uropods absent, sockets present ( Lyreididae ) or absent ( Raninidae ). Locking mechanism absent in Raninidae ; present in Lyreididae as pair of hook-like, short, stout or elongated projections arising from episternite 5, distally with double peg, which firmly fits into deep sockets in latero-posterior extended corners of abdominal somite 6.

Chelipeds generally robust, variously modified, homochelous, homodontous; arthrodial cavities large, placed laterally or ventrolaterally; basis-ischium short, fused with merus; propodus varying from short, inflated, flattened, armed with long, sharp spines on upper, lower margins to elongated, narrow, unarmed; fingers usually with teeth of prehensile borders joining alternately, or with several long spines ( Cyrtorhininae ); fixed finger diminutive to long, often deflected. P2‒P4 robust or slender, rather long, at least propodus, dactylus markedly modified; dactylus paddle shaped, lanceolated, or falciform; P4 slightly subdorsal, P5 dorsal, slightly to strongly reduced (may be filiform in Lyreididae ), generally matching carapace margins.

Pleopod 1 absent in females. G1, G2 variously shaped. Gills: 8 pairs, rarely 7 ( Symethinae ).

Respiratory mechanism strongly specialised. Absence of Milne-Edwards openings, except possibly in Marylyreidinae n. subfam. Respiratory inhalant, exhalant currents through strongly, variously modified frontal region, posterior branchial orifices; water flows along flanks of carapace.

Remarks. Table 7 lists the genera included herein in Raninoidea . Although variously shaped, the raninoid thoracic sternum (except Cyrtorhininae ) shows a small, lanceolated anterior element, followed by a rather large shield formed by the well-developed sternite 4. The crown-shaped element only comprises sternite 3, sternites 2 and 1 being anteriorly, not visible dorsally and not participating in the formation of the sternal plastron. The crownshaped anterior sternites in extant raninoids resemble to some extent those found in extant dynomenids, but the crown does not include sternite 3 in the latter (Guinot 2008). The posterior sternites are extremely narrow in all raninoid families, and as a result, the P2, P3 and P4 arthrodial cavities are closely contiguous. The P1 coxae also are close to each other in Cyrtorhininae .

The spermathecae of Raninoidea appear to open anteriorly on sternite 7 rather than at the extremities of sternal suture 7/8, as in other Podotremata. The spermathecal chamber, however, is still formed by the separation of the two laminae which compose endosternite 7/8, which is not a major departure from the typical podotreme configuration ( Tavares & Secretan 1993), as explained by Hartnoll (1979). The spermathecal apertures are located in proximity to the female gonopore on the P3 coxae. The spermathecal apertures are close to each other and recessed in a medial pit in all raninoids, but more superficial and hooded in the Symethinae .

Pleopod 1, which is present in the basal Podotremata (Dromioidia, Homoloidia), is absent in raninoid females, as in Cyclodorippoidia and Eubrachyura.

The variously shaped male sexual gonopods indicate a strong diversity. In all Raninoidea , the G1 is partially open, it does not form a complete tube, and is foliaceous in Notopodinae ; the G2 is long or short. The two G1 are close to each other and act together. Their apices, which are not in contact medially, may nevertheless inseminate the two closely placed spermathecal apertures. The sperm, ejaculated from the penis to the base of the G1 and picked up by the spoon-like G2 to be placed in the distal part of the G1, is transferred through the G1 ejaculatory channel into the spermathecae.

Antonioranina n. gen. (†) Bicornisranina Nyborg & Fam, 2008 (†) Bournelyreidus n. gen. (†) Cosmonotus Adams & White in White, 1848 (†, #) Cristafrons Feldmann, Tshudy & Thomson, 1993 (†) Cyrtorhina Monod, 1956 (#) Eosymethis n. gen. (†) Eumorphocorystes van Binkhorst, 1857 (†) Heus Bishop & Williams, 2000 (†) Lianira Beschin, Busulini, De Angeli, Tessier & Ungaro, 1991 (†) Lophoranina Fabiani, 1910a (†) Lophoraninella Glaessner, 1945 (†) Lovarina Beschin, Busulini, De Angeli, Tessier & Ungaro, 1991 (†) Lyreidina Fraaye & Van Bakel, 1998 (†) Lyreidus De Haan, 1841 (†, #) Lysirude Goeke, 1986 (†, #) Macroacaena Tucker, 1998 (†) Marylyreidus n. gen. (†) Neoraninella Hu & Tao, 1996 (incertae sedis) (†) Notopella Lőrenthey in Lőrenthey & Beurlen, 1929 (†) Notopoides Henderson, 1888 (†, #) Notopus De Haan, 1841 (†, #) Notosceles Bourne, 1922b (†, #) Ponotus Karasawa & Ohara, 2009 (†) Pseudorogueus Fraaye, 1995 (†) Quasilaeviranina Tucker, 1998 (†) Ranidina Bittner, 1893 (†) Ranilia H. Milne Edwards, 1837 (†, #) Raniliformis Jagt, Collins & Fraaye, 1993 (†) Ranina Lamarck, 1801 (†, #) Raninella A. Milne Edwards, 1862 (†) Raninoides H. Milne Edwards, 1837 (†, #) Remyranina Schweitzer & Feldmann, 2010a (†) Rogueus Berglund & Feldmann, 1989 (†) Symethis Weber, 1795 (#) Symethoides n. gen. (†) Sabahranina Collins in Collins, Lee & Noad, 2003 (incertae sedis) (†) Tribolocephalus Ristori, 1886 (†) Umalia Guinot, 1993b (†, #) Vegaranina n. gen. (†)

There are eight pairs of gills in Raninoidea , all arranged in a vertical position the anteriormost two pairs reduced in size but large enough to be observed and be functional ( Bourne 1922b: 56; Goeke 1981: 978). There are only seven pairs in Symethinae , with the anteriormost two pairs greatly reduced.

Sexual dimorphism is relatively indistinct in the abdomen, which is not much widened in females. The chelae are homeomorphic in males and females. At least in males of Ranina , which are larger than females, the anterolateral carapace teeth are more developed, the chelae are larger and setae on the P1 propodus and dactylus different ( Fielding & Haley 1976: fig. 4). In Ranina ranina ( Linnaeus, 1758) sexual dimorphism is observed from the instar I pleopods, on abdomens of individuals over 34 mm in length and in chelipeds of individuals longer than 70 mm. Uropods of males degenerate and disappear by instar III. The puberty moult is estimated to be linked to a carapace length of 40–45 mm (Minagawa 1993a).

Ontogenetic changes may be present in raninoideans. Sakai (1937: fig. 45a–c) illustrated size changes in the anterior teeth of the carapace of Ranina ranina : small and simple in juvenile females, well developed and divided into three equal teeth in adult females, much stronger and wider in adult males. Ranina ranina , which is widely spreaded, might comprise several distinct species so information on this intraspecific variation may be misleading. Ontogenetic changes in functional morphology may be apparent in cuticle microstructures, and Savazzi (1981) documented allometric changes in a number of terraces during growth in Lophoranina spp. from Eocene strata in northern Italy.

The close resemblance between Raninoidea and the ‘mole crabs’ or ‘sand crabs’ (Anomura, Hippoidea) is due to parallel evolution and convergence, with similar high specialisation for burying/back-burrowing activities into sand, tail first (elongated body adapted to backing into soft sediment and modified legs). Hippoids markedly differ from raninoids in having uropods and a combination of leg movements with simultaneous tail flipping and uropod beating for swimming and digging ( Faulkes & Paul 1997 a, b, 1998).

Date of publication of the Raninoidea De Haan . The year of publication of Raninoidea De Haan has been cited either as 1839 (e.g., Manning & Holthuis 1981; Martin & Davis 2001; Guinot et al. 2008; Ng et al. 2008; De Grave et al. 2009; Schweitzer et al. 2010) or as 1841 (e.g., Wright & Collins 1972; Guinot 1993b; Tucker 1998; Feldmann et al. 2008). Crustaceans in Fauna Japonica by De Haan have been published in several issues (‘livraisons’) between 1833 and 1850 ( Holthuis & Sakai 1970). The diagnosis of the taxon ‘Raninoidea’ can be found on p. 136, thus dated as 1841, but the name first appeared on p. 102 (i.e., in 1839) in a rather extensive comparison with ‘Dromiacea’. This earlier indication suffices as a valid use, being in accordance with the provisions of the International Code of Zoological Nomenclature ( ICZN 1999), and thus the correct date should be 1839.

Historical account of extant Raninoidea . Early illustrations of raninoid crabs are those of Rumphius (1705), who depicted Ranina ranina ( Linnaeus, 1758) [as Cancer Raniformis [sic]; see Rumphius 1705: 13, pl. 7, figs. T, V] and Notopus dorsipes ( Linnaeus, 1758) [as Pediculus marinus [sic]; Rumphius 1705: 29, pl. 10, fig. 3) ( Holthuis 1959: 107, 108, photo 8, figs. 8, 9). When erecting the Cancer raninus, Linnaeus (1758: 625) , followed later by Lamarck (1801: 156; 1818: 224), who established Ranina , also alluded to the frog-like shape of these strange animals, which were initially placed within the Insecta Aptera. Some unusual characters of Raninoidea (e.g., body shape, cuticle ornament, short and unfolded abdomen, keel-like posterior sternites, cryptic spermathecal apertures, respiratory structures) are extensive modifications connected with a highly specialised burying/back-burrowing behaviour (see Morphology of the Raninoidia below). This partially explains why their taxonomic status has been problematic and varied over time. Even to this day, the raninoid lineage is subject of ongoing debate.

The raninids were considered either as ‘Crustacés Pédiocles’, a group which also comprised Albunea Weber, 1795, Hippa Fabricius, 1787 , Scyllarus Fabricius, 1775 , Palaemon Weber, 1795 , and Squilla Fabricius, 1787 ( Lamarck 1801) , or as ‘Brachyuri among the Oxyrynchi’, which included Corystes Bosc, 1802 , Dorippe Weber, 1795 , Maja Lamarck, 1801 (as Maia ) and Orithyia Fabricius, 1798 ( Latreille 1802: 28; 1806: 43; 1810: 98). Others ( Latreille 1825: 273; Berthold 1827: 259) ranked them in the brachyuran tribe Notopoda Latreille, 1817 (pp. xiii, 24, 25), which comprised various crabs with dorsal last pereiopod(s) such as Dorippe , Dromia Weber, 1795 , and Homola Leach, 1815 , but Guérin (1832: 285) subsequently excluded Ranina Lamarck, 1801 , from this tribe. Alternatively, they were assigned to ‘Astacoïdes’ within the family ‘Oxyrhynques’, together with Dorippe , Leucosia Weber, 1795 , Maja and Orithyia ( Duméril 1806) , considered as ‘Macroures’ among the ‘Paguriens’ ( Lamarck 1818: 197, 224), or interpreted as a special tribe within the Macrouri [sic] ( Latreille 1831: 368; see below). Desmarest (1825: 138) regarded Ranina as a brachyuran.

Conversely, H. Milne Edwards (1837: 167, 190) attributed the tribe ‘Raniniens’ (together with two other podotreme tribes, ‘Dromiens’ and ‘Homoliens’) to the ‘Décapodes Anomoures’ within the family ‘Aptérures’ (i.e., without tail fan), as opposed to the ‘Ptérygures’ (i.e., with biramous uropods and a tail fan) comprising ‘Paguriens’, ‘Hippiens’ and ‘Porcellaniens’. Dana (1852: 54, 402, 403, under the name of Raninidea) and Henderson (1888: ix, 26) also referred all podotreme crabs, including Raninidae , to Anomura.

Another interpretation was to view raninids as true crabs (i.e., Brachyura ), and for a considerable period of time they were attributed to Oxystomata De Haan. The first author to do so was De Haan (1839: 102; 1841: 119, 136–140; 1850: xvii), who established the taxon Raninoidea . He was followed by several carcinologists ( Ortmann 1892: 557, 559, 574; Alcock 1896: 135, 136, 288; Ihle 1918: 1, 294; Sakai 1937: 165, 168; Balss 1957: 1608, 1616).

Alphonse Milne-Edwards & Bouvier (1902: 7), however, excluded Raninoidea from Oxystomata, thus confirming the doubt already expressed by Boas (1880: 2002). As an outcome of his remarkable study, Bourne (1922b: 55) ranked Raninidae with the Brachyura as a special tribe, Gymnopleura , ‘equivalent to the Dromiacea, Brachygnatha and the rest of the Oxystomata.’ The separation of the raninoid crabs in a tribe next to other Brachyura was followed by several authors, including Rathbun (1937a), Gurney (1942), Garth (1946), Richardson & Krefft (1949), Barnard (1950), Gordon (1963, 1966), Monod (1956), Waterman & Chace (1960), Tyndale-Biscoe & George (1962), Bennett (1964), Sakai (1965, 1976), Pichod-Viale (1966), Forest & Guinot (1966), Takeda & Miyake (1970), Serène & Umali (1972), Fielding & Haley (1976), Hartnoll (1968, 1975, 1979), Goeke (1980, 1981), Dai & Xu (1991), Dai & Yang (1991), Chen & Xu (1991) and Watabe (2007).

For Števčić (1973: 631) ‘the raninids started their evolution from highly developed crabs’, and ‘their subsequent evolutionary pathway was regressive in both a morphological and ecological sense’, but later Števčić (2005: 33) placed Raninoidea ‘at the end of the dromiacean hierarchical system’. Similarly, Hartnoll (1979: 75) regarded the raninoids as, ‘the most advanced of the primitive Brachyura .’A reinterpretation of raninoid crabs became possible only after the discovery of an internalised spermatheca ( Gordon 1963: 53, figs. 12, 13; 1966: 343, figs. 1–3; Hartnoll 1975, 1979), a primitive axial skeleton ( Drach 1950: 2; Gordon 1966: 350), a special cephalic (ocular) configuration close to that of Dromia ( Pichod-Viale 1966: 1266) , the frequent incomplete tubulation of G1 and the relative length of G2 ( Gordon 1966: 348; Serène & Umali 1972: figs. 5, 6; Guinot 1979: 232, fig. 62E–H).

The presence of coxal female sexual openings, plus the presence of a paired spermatheca, added to the abovementioned primitive features that all indicate a podotreme condition, led to the inclusion of Raninoidea in Podotremata, next to Dromiacea, Homoloidea and Cyclodorippoidea ( Guinot 1977: 1050; 1978: 237; 1993b: 1324; Guinot & Bouchard 1998: 639; Guinot & Tavares 2001: 524, table 16; Guinot & Quenette 2005: 312).

Another turning point in classification was the abandonment of the concept of the Podotremata, based, for the most part, on molecular results. Spears & Abele (1988: 2 A) removed Dromiidae from Brachyura , arguing that dromiids ‘branch very early, prior to the Anomura.’ Concluding that ‘there is no molecular support [...] for the division Podotremata (sensu Guinot), which groups raninids and dromiids together on the basis of a similar gonopore location’, Spears et al. (1993: 456) proposed to abandon the taxon Podotremata and set Raninidae at the lower limit within Brachyura . This interpretation of the molecular data was based on the study of only four species of Podotremata, without considering any dynomenid, homolodromiid, homolid, latreilliid, cymonomid or cyclodorippid taxa. Additional investigations led Spears & Abele (oral statement in 2nd European Crustacean Conference, Liège 1996; 1996: 14bis) to another major change by considering Dromiacea as true brachyurans to become the sister group of the Homoloidea and concluding Podotremata to be polyphyletic. Thus, Raninoidea (together with Cyclodorippoidea) became basal members of Eubrachyura, in which they formed a special subsection, Raninoida, consisting of only two families, Raninidae and Symethidae ( Martin & Davis 2001: 49, 74). Results of Ahyong et al. (2007) showed that the ‘ Hypoconcha ’ sequence of Spears et al. (1993) represented a diogenid hermit crab rather than a brachyuran, so the Hypoconcha -Anomuran hypothesis should be abandoned ( Ahyong et al. 2007: 582).

The classification of Martin & Davis (2001) has been followed by a number of palaeontologists ( De Angeli & Beschin 2001; Feldmann 2003; Collins et al. 2003; Collins & Jakobsen 2004; De Angeli & Garassino 2006b; Schweitzer et al. 2010), who treated raninoids as eubrachyuran crabs. This placement of Raninoidea (and Cyclodorippoidea) within Eubrachyura was in contradiction with De Grave et al. (2009), who excluded section Raninoida (as well as section Cyclodorippoida) from Eubrachyura and placed them more basally, next to section Dromiacea. It is obvious that such a major change, all within a year, reflects the disagreement with how these crabs should be classified as well as the failure of the non-recognition of the Podotremata.

A molecular study by Ahyong et al. (2007), based on a larger sample of species and genes, suggested a paraphyletic Podotremata; and three podotreme sections, Dromiacea, Raninoida and Cyclodorippoida were proposed ( Ahyong et al. 2009; Ng et al. 2009: fig. 4). In consideration of the level of generality of the characters, however, these ‘sections’ are not equivalent to the ‘section’ Eubrachyura (see Phylogeny of the Raninoidia below).

The study of well-preserved fossils, for which the family Cenomanocarcinidae ( Guinot et al. 2008: 682, 712) was erected, and a brief discussion of the status of Raninoidea , formed the first step of the present revision. Neontologists and, even less so, molecular scientists would be unable to appreciate the extreme diversity and complexity of an ancestral group, especially when fossils are added, as in the case of raninoids. The practical necessity to consider new ranks therefore becomes clear so that a resolved phylogeny accommodates ancestral taxa in classifications. We therefore continue to recognise two sections in Brachyura , namely Podotremata and Eubrachyura. The former comprises four subsections, covered by earlier diagnoses: Dromioidia De Haan, 1833 (= Dromiacea De Haan, 1833, emend.), Homoloidia De Haan, 1839, Cyclodorippoidia Ortmann, 1892, and Raninoidia De Haan, 1839 (Guinot et al. in press). The section Eubrachyura de Saint Laurent, 1980, its sister group, comprises two subsections, Heterotremata Guinot, 1977, and Thoracotremata Guinot, 1977. The Raninoidia contains two superfamilies, Palaeocorystoidea (extinct only) and Raninoidea (both fossil and extant; Table 1).

The name Notopterygia Latreille, 1831 . In his Cours d’entomologie, Latreille (1831: 368) established, within the Macrouri, the tribe Notopterygia , providing a description and type designation, viz. ‘albunea scabra de Fabricius, ou le cancer raninus de Linné ’. The name of his new tribe was based on the shape of all the legs, at the same time ending in ‘fins’ and arranged in two rows, the posterior being dorsal (‘ tous les pieds … à la fois terminés en nageoire et disposés sur deux rangs, les deux ou quatre postérieurs étant dorsaux’). Latreille (1831: 328, 369) clearly distinguished the Notopterygia from the other Macruri on the lack of uropods (forming the tail fan characteristic of Decapoda other than Brachyura ) and, in particular, delimited it well from a second tribe, the ‘Hippides’. Latreille (1831: 369) included in Notopterygia the fossil species Lophoranina aldrovandii ( Ranzani, 1818) . The definition was subsequently cited by Jourdan (1834: 147) and the same classification was followed by Lucas (1840: 154, 155). The taxon Notopterygia was quoted only by Bate (1888: 4) in a table showing previous classifications. In a report to the Linnean Society (December 1921), the name Gymnopleura was proposed by Bourne (1922: 55); Stebbing (1922: 108) remarked that Gymnopleura was preoccupied by the name Notopterygia (quoted previously by Stebbing 1908: 17). Bourne (1922a: 108), in a letter to the editor of Nature, wrote that, ‘it seems that my proper course will be to withdraw the name ‘Gymnopleura’ and substituted that of ‘ Notopterygia , Latreille’ in an addendum of the printer paper’. Finally, in a footnote, Bourne (1922b: 55) decided not to use Latreille’s name so as to avoid confusion. The correct name Gymnopleura Bourne, 1922 , to accommodate a separate tribe of crabs with exposed pleurites, was published just as it was. The name Gymnopleura was used by several authors, even fairly modern ones (see synonymy), but later was abandoned as a junior synonym of Raninoidea De Haan, 1839 .

As far as we are aware, the case of the nomen ‘ Notopterygia Latreille, 1831 ’ has never been discussed. The nomen Notopterygia is not formed from the stem of an available generic name. Thus, following ICZN Article 11.7.1.1, it could only be considered available if taken above superfamily rank, thus outside the family group. The Code does not cover names of ranks above the level of superfamily, and the question is in study (Guinot et al. unpublished).