A Puzzling Frog Crab \(Crustacea: Decapoda: Brachyura\) from the Early Cretaceous Santana Group of Brazil: Frog First Or Crab Fi

Home , Homoloidea, Necrocarcinidae, Portunoidea, Ranina, Raninidae, Raninoida

Journal of Systematic Palaeontology, 2015 Vol. 13, No. 2, 153–166, http://dx.doi.org/10.1080/14772019.2013.871586

A puzzling frog crab (Crustacea: Decapoda: Brachyura) from the Early Cretaceous Santana Group of Brazil: frog first or crab first? Javier Luquea,b* aDepartment of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada; bSmithsonian Tropical Research Institute, Balboa–Ancon 0843–03092, Panama, Republic of Panama (Received 29 April 2013; accepted 30 September 2013; first publihsed online 10 April 2014)

The evolutionary origin of frog crabs (Raninoida) remains puzzling partly due to their astonishing morphological disparity, ranging from broad and heavily ornamented ‘crab-like’ extinct families (necrocarcinids and allies), to elongate and smoother ‘frog-like’ extant ones (raninids and allies). However, an ancient Cretaceous clade (Palaeocorystidae) displays a combination of plesiomorphic and apomorphic traits that might advocate for either evolutionary scenario: from ‘crab-like’ to ‘frog-like’, or vice versa. This lack of agreement is partly fuelled by the scarcity of Early Cretaceous fossils, a time from which the first raninoidans are known. A close re-examination of an Early Cretaceous fossil from the Santana Group of Brazil, Araripecarcinus ferreirai Martins-Neto, 1987, combined with phylogenetic analysis including all main clades of podotreme crabs, reinforces its raninoidan condition, and rejects the initial hypothesis of a Portunoidea affinity. Furthermore, comparisons with other raninoidans support the hypothesis that a more ‘crab-like’ body plan is the plesiomorphic condition for raninoidans, and that the ‘frog-like’ architecture of Palaeocorystidae, and perhaps the Raninoidea as a whole, reflects a derived condition related to a specialized burrowing lifestyle. Phylogenetic analyses are fundamental to evaluate the position of Palaeocorystidae with respect to raninoidean and necrocarcinid-like families, helping to better resolve the Raninoida evolutionary tree of life, and to gain a broader understanding on their relatedness by common ancestry throughout geological time. Keywords: Albian; evolution; Neotropics; Raninoida; Raninoidia; South America

Introduction partly due their astonishing morphological disparity, ranging from broad and heavily ornamented ‘crab-like’ fami- The particular body plan of extant frog crabs has puzzled lies (necrocarcinids and allies), to elongate and smoother scientists since the time of Linnaeus, resulting in multiple ‘frog-like’ ones (raninids and allies). Furthermore, an afﬁliations with ‘higher’ and ‘podotreme’ brachyuran intermediate group, the palaeocorystids, combines plesio- crabs, anomurans, macrurans, and even apterous insects morphic and apomorphic traits seen in both clades, and (Linnaeus 1758; Lamarck 1801; Latreille 1802; Milne their phylogenetic afﬁnities are still debated. In addition, Edwards 1837; Dana 1852; Ortmann 1892; Alcock 1896; the Early Cretaceous has been deemed as the time where

Downloaded by [University of Alberta] at 22:49 10 January 2015 Bourne 1922; Glaessner 1960; 1969; Stev cic 1973; 1995; the main raninoidan lineages diversified (Karasawa et al. Martin & Davis 2001). They are a group of true crabs, or 2011; Luque et al. 2012; Van Bakel et al. 2012a), but their Brachyura, whose modern representatives are adapted for scarce fossil record compared to that in the Late Creta- burrowing in soft to gravelly substrates. Their diagnostic ceous biases our understanding of the polarity of change traits, once considered to reflect an ancestral condition of certain traits, and thus our understanding of their relat- (e.g. elongate carapace, pleon exposed dorsally, narrow edness by common ancestry throughout geological time. sternum and flattened legs), are now thought to be derived The late Early Cretaceous Santana Group in Brazil, adaptations for their burrowing lifestyle, and therefore South America is an astonishing fossil-bearing deposit convergent between several non-related superfamilies of recognized worldwide for extraordinary preservation of digging anomuran and brachyuran crabs (Borradaile marine and terrestrial invertebrates, vertebrates and plants 1903; Bourne 1922; Gordon 1966; Glaessner 1969; (Maisey 1991). Despite the many arthropods found there, Stev cic 1973; Williams 1974; Abele & Felgenhauer 1982; only one species of true crab or Brachyura, Araripecarci- Gaten 1998; Dawson & Yaldwing 2000; Stev cic 2005). nus ferreirai, has been reported so far. Its holotype and The evolutionary origin of raninoidans remains puzzling sole specimen was originally described as a dorsal

*Corresponding author. Email: [email protected]

carapace of a portunid crab, a group of higher brachyurans Raninoida De Haan, 1839 known for their ability to swim with paddle-like posterior ?Necrocarcinidae Forster,€ 1968 legs (Martins-Neto 1987; Maisey 1991; Maisey & Genus Araripecarcinus Martins-Neto, 1987 Carvalho 1995). However, a re-examination of this specimen has revealed that it is neither a portunid crab nor a Type species. Araripecarcinus ferreirai Martins-Neto, dorsal carapace with a flattened last pair of legs. This was 1987, by monotypy. first noticed by Guinot & Breton (2006) who accurately Emended diagnosis. Carapace subcircular in outline, proposed that Araripecarcinus belonged to Raninoidea, a nearly as wide as long, as seen in Necrocarcinidae, Ceno- group of crabs only distantly related to portunids (Guinot manocarcinidae Guinot et al., 2008; Orithopsidae Schweit- et al. 2013). Karasawa et al. (2008) discussed the ventral zer et al., 2003, and Camarocarcinidae Feldmann et al., orientation of the Araripecarcinus type specimen, and 2007; maximum width near to midlength; pterygostome based on the shared elongate buccal cavity, the narrow broad, vaulted, crest inconspicuous, surface granulated; sternum and the posteriorly extended abdomen, allied it anterolateral and posterolateral margins convex, both with Raninidae De Haan, 1839. Since then, Araripecarci- apparently lacking spines; cervical groove reaching ventral nus has been regarded as a raninoidan/raninoidian, carapace; buccal cavity elongated, about half the carapace although with unclear affinities (Schweitzer et al. 2010; length. Thoracic sternum narrow; S3 distinct ventrally, Luque et al. 2012; Van Bakel et al. 2012a; Guinot et al. wider than long; S4 flattened mesially, lateral margins sub- 2013), which calls for re-examination of the type material, parallel and slightly convex; E4 longer than wide, slightly and discussion of the species’ systematic relationship with ovate distally, forming with lateral margins of S4 an angle other raninoidans. of 120; suture 4/5 incomplete; S5 similar in shape to This is the first attempt to place Araripecarcinus in syn- S4; suture 5/6 incomplete; S6 separated in anterior and pos- thetic and cladistic contexts, and discuss its implications terior plates by a weak, transverse break point; sterno-coxal for frog crab phylogenetic relationships. depression absent; thoracic sexual openings absent; sternal pleon locking mechanisms on E5 absent in holotype. Cheli- Institutional abbreviations peds (Ch) isochelous; P2 and P3 the longest of all pereiopods, similar in size; P4 nearly half P2–P3; P5 the AMNH: American Museum of Natural History, New smallest, very reduced, apparently sub-dorsal. York, United States; IMG: Museo Geologico Nacional Jose Royo y Gomez, Servicio Geologico Colombiano Occurrence. Late Early Cretaceous (Albian) of the (formerly INGEOMINAS), Bogota DC, Colombia; Araripe Basin, Brazil. IRScNB: Institut royal des Sciences naturelles de Belgi- que, Brussels, Belgium; USNM: National Museum of Remarks. The original assignment of Araripecarcinus Natural History, Smithsonian Institution, Washington, within Portunoidea Rafinesque, 1815, was founded on the DC, USA; UF: Invertebrate Paleontology Division, Flor- presumed possession of a P5 adapted for swimming as ida Museum of Natural History, University of Florida; seen in most portunoids, and different enough from the USP: Instituto de Geociencias da Universidade S~ao Paulo, ‘flattened and foliaceous’ pereiopods seen in extant mem- S~ao Paulo, Brazil. bers of Raninoidea (Martins-Neto 1987, p. 408). However, what was considered to be flattened sclerites of P5, actually

Downloaded by [University of Alberta] at 22:49 10 January 2015 correspond to the carpus and the apparently flat propodus Anatomical abbreviations of P4, whereas P5 is very reduced and apparently carried A6: sixth abdominal somite; Ca: carpus; Cg: cervical subdorsally (Figs 1B, 2A). In addition, the ‘portunid bran- groove; Ch: cheliped; CI: consistency index; Cx2–Cx4: chial lobes’ depicted by Martins-Neto (1987,fig.2),are coxa of second to fourth pereiopods; Cx Ch: coxa of che- the arthrodial cavities of the chelipeds; the ‘epibranchial’ liped; Cx mxp3: coxa of third maxilliped; Da: dactylus; and ‘mesogastric’ regions are the pterygostome and the Ds: dorsal spine; E: compound eye; E4–E7: episternites buccal cavity respectively; and the ‘urogastric’, ‘cardiac’ four to seven; Ex mxp3: exopod of third maxilliped; Me: and ‘intestinal regions’ are part of the thoracic sternum merus; Mxp3: third maxilliped; P2–P5: second to fifth (Figs 1A, B, 2A, B). Furthermore, Martins-Neto stated that pereiopods; Pr: propodus; ?Pr: ?propodus; Rs: rostral Araripecarcinus “is clearly related to the torynommid spine; S3–S8: sternites three to eight. genus Mithracites from the Aptian of England” (Martins- Neto, in Maisey 1991,p.411).Currently,Mithracites Gould 1859, is regarded as closer to homoloidans than to Systematic palaeontology torynommoidans (Guinot & Tavares 2001; Stev cic 2005; Karasawa et al. 2011; Schweitzer & Feldmann 2011;Van Decapoda Latreille, 1802 Bakel et al. 2012b; Guinot et al. 2013), and based on the Brachyura Linnaeus, 1758 diagnostic traits seen in the type material of A puzzling Cretaceous frog crab from Brazil 155

Figure 1. Raninoida. A, B, Araripecarcinus ferreirai Martins-Neto, 1987, Albian of Brazil; A, ventral view of holotype USP (GP/1T 1477); B, cast of holotype coated with ammonium chloride. C, Necrocarcinidae, Corazzatocarcinus sp., ventral view of specimen UF110982, Cenomanian of Lebanon. D, Cenomanocarcinidae, Cenomanocarcinus sp., ventral view of specimen IGM p880291, Turo- nian of Colombia (Luque et al. in progress). Abbreviations: A6, sixth abdominal somite; Ca, carpus; Cg, cervical groove reaching ventral Downloaded by [University of Alberta] at 22:49 10 January 2015 carapace; Ch, cheliped; Da, dactylus; Ex mxp3, exopods of third maxilliped; Me, merus; Mxp3, third maxillipeds; P2–P5, pereiopods two to ﬁve; Pr, propodus.

Araripecarcinus, afﬁliation with portunoids, homoloids or anterior margin of E4 an angle of nearly 120 (Fig. 2B). torynommoids is untenable. Moreover, its palaeogeographical and stratigraphical Among podotreme crabs, Araripecarcinus traits are range contrast with those of typical camarocarcinids, reminiscent of those present in the raninoidan families exclusively known from Paleocene rocks of North Camarocarcinidae and Necrocarcinidae, especially the Dakota, Greenland and Denmark (Holland & Cvancara roundish carapace outline, the morphology of the thoracic 1958; Feldmann et al. 2007; Guinot et al. 2008; Van sternum, and the cervical groove reaching ventrally Bakel et al. 2012a), further casting doubts on any camaro- (Fig. 1A, B). Araripecarcinus, however, lacks the grooved carcinid relationship. This does not rule out that camaro- pterygostome seen in camarocarcinids, with a long blunt carcinids might have Cretaceous representatives from low crest, the strongly concave thoracic sternum and the latitudes, but no such fossils have been found to date. sterno-abdominal depression (Van Bakel et al. 2012a). Its The thoracic conﬁguration of Araripecarcinus is puz- episternites are more broadly spaced from each other than zling. Its sternite 3 is covered anteriorly by matrix, pre- other palaeocorystoids, and the S4 has subparallel and cluding the study of anterior sternites. The exposed part of slightly convex lateral margins and forms with the sternite 3 is longer than in many other raninoidans. 156 Javier Luque

Figure 2. Raninoida. A, B, Araripecarcinus ferreirai Martins-Neto, 1987, cast of holotype USP (GP/1T 1477), Albian of Brazil; A, ven- Downloaded by [University of Alberta] at 22:49 10 January 2015 tral view showing the position of chelipeds, pereiopods, and abdominal somite 6; B, close-up of A, showing details of the thoracic sternum. C, Camarocarcinidae, Camarocarcinus arnesoni Holland & Cvancara, 1958, hypotype USNM 103624, ventral view, Upper Cretaceous of North Dakota, USA. D, Orithopsidae, Silvacarcinus laurae Collins & Smith, 1993, ventral view of holotype IRScNB TCCI 6115, Lower Eocene (Ypresian) of Belgium (reproduced from Van Bakel et al. 2012, ﬁg. 21a, with permission from Magnolia Press). Abbreviations: A6, sixth abdominal somite; ?Pr, ?propodus of P4; Ca, carpus; Ch, cheliped; Cx mxp3, coxa of third maxilliped; Cx2–Cx4, coxae of P2 to coxa of P4; Da, dactylus; E4–E7, episternites four to seven; Me, merus; P2–P5, pereiopods two to ﬁve; Pr, propodus; S3–S7, sternites three to seven.

However, sternal features vary considerably among fami- accommodation of a well-developed articular condyle of lies and genera, and a similar condition as in Araripecar- P1, and can be considered as an autapomorphy for Arari- cinus can be seen in specimens of Necrocarcinus pecarcinus among raninoidans. Following the works of labeschei (Eudes-Deslongchamps, 1835), as illustrated in Karasawa et al. (2011) and Van Bakel et al. (2012a), the Karasawa et al. (2011, fig. 10B), Orithopsis tricarinata presence of a double protrusion mechanism on E5 for (Bell, 1863) in Van Bakel et al. (2012a, fig. 22A, D), and abdomen holding seen in Orithopsidae and Cenomanocar- Planocarcinus johnjagti in Bermudez et al.(2013, fig. 8I). cinidae, their broad S4 with large and wide E4 (Fig. 3), The narrowness of Araripecarcinus sternite 4, particularly their generally sub-hexagonal carapaces, and the cervical in the posterior portion, might be related with groove ending anterior to the spinose anterolateral A puzzling Cretaceous frog crab from Brazil 157 Downloaded by [University of Alberta] at 22:49 10 January 2015

Figure 3. General sternal configuration in Araripecarcinus Martins-Neto, 1987, and representatives of the eight terminals of Raninoida (Figs 4, 5). A, Araripecarcinus ferreirai Martins-Neto, 1987 (Figs 1A, B, 2A, B). B, Camarocarcinidae, Camarocarcinus arnesoni Hol- land & Cvancara, 1958 (Fig. 2C). C, Necrocarcinidae, Necrocarcinus labeschei (Eudes-Deslongchamps, 1835) (after Karasawa et al. 2011, fig. 10B). D, Cenomanocarcinidae, Cenomanocarcinus sp. (Fig. 1D). E, Orithopsidae, Silvacarcinus laurae Collins & Smith, 1993 (Fig. 2D). F, Palaeocorystidae Lorenthey in Lorenthey & Beurlen, 1929, Notopocorystes stokesii (Mantell, 1844) (after Van Bakel et al. 2012, fig. 37A). G–I, Raninoidea; G, Lyreididae, Lyreidus tridentatus de Haan, 1841 (after Feldmann & Schweitzer 2007, fig. 4B); H, Raninidae, Raninoides sp.; I, Symethidae, Symethis sp. Abbreviations: Ch, cheliped; P2, second pereiopod. The circles indicate the approximate location of coxae of Ch and P2.

margins, rule out affiliation with Araripecarcinus. Arari- sternites 6 and 7, at first, appears to be complete. How- pecarcinus ventral architecture is more reminiscent of ever, that separation corresponds to a fracture zone related some necrocarcinid-like taxa, especially that of Planocar- to a weak point in the thoracic sternum (Van Bakel, pers. cinus Luque et al. 2012. Both taxa have E4 and E5 sepa- comm. 2012), with its sutures only expressed laterally. rated from one another (Bermudez et al. 2013, fig. 8I). In Whether or not this is the case in Araripecarcinus is hard some raninoidans such as Notopocorystes stokesii (in Van to tell since the specimen is likely a fragmented exuviae Bakel et al. 2012, fig. 59A, B), the suture between with disarticulated thoracic elements. 158 Javier Luque

Raninoidans s.l. have diverse sternal morphologies, and The sternal suture 3/4 is not seen. The S4 is semi-rectan- Araripecarcinus appears not to be an exception. The over- gular and slightly longer than wide, with its anterior por- all sternal similarities with Sphaerodromiidae Guinot & tion sub-square, shallowly depressed axially, bearing Tavares, 2003 (see also Schweitzer & Feldmann 2010) slightly convex sub-parallel lateral margins, and forming and other podotremes would not be that surprising, if with the lateral margins of E4 an angle of 120 some early raninoidan clades might have shared more ple- (Figs 2B, 3A). The E4 is longer than wide, slightly ovate siomorphies with other podotreme clades than more distally, and approximately as long as the lateral margin derived raninoidans do. Araripecarcinus might well of S4; the sternal suture 4/5 is incomplete; the S5 is simi- belong to the same stock as planocarcinids or paranecro- lar in shape to S4, but slightly wider; the sternal suture 5/6 carcinids, but its unknown dorsal carapace, together with is incomplete; the anterior portion of S6 is apparently the poorly known sternal architecture of planocarcinids fused with S5, and separated from its posterior portion by and paranecrocarcinids (Feldmann et al. 2007; Jagt et al. a weak, transversal fracture point (Fig. 2B, white double 2010; Luque et al. 2012; Van Bakel et al. 2012a), arrow). The E6 is approximately as long as E4; the sternal obscures its suprageneric placement. suture 6/7 is unclear; the S7 is reduced, somewhat disarticulated from S6; the E7 is longer than wide; and the S8 Araripecarcinus ferreirai Martins-Neto 1987 is unknown. The holotype of Araripecarcinus lacks a ster- (Figs 1A, B, 2A, B) nocoxal depression, as well as thoracic sexual openings. Neither spermathecal apertures, nor sternal pleon locking Emended diagnosis. As for genus. mechanisms, are recognizable in the holotype. Its A6 is Material. Series of photos and cast of the holotype and wider than long, with lateral margins convergent posteri- sole specimen USP (GP/1T 1477), deposited in the Insti- orly, and posterior margin apparently concave. tuto de Geociencias da Universidade S~ao Paulo, S~ao The Ch are isochelous; with the propodus longer than Paulo, Brazil. wide, bearing a manus moderately inflated, and with the pollex and dactylus poorly preserved; its merus is about Measurements. Carapace maximum length: 10.3 mm; twice as long as wide, wider anteriorly, and bearing a few width, 10.4 mm. tubercles externally. The P2 is partly preserved; its coxa is large, nearly as wide as long, and about the same width Occurrence. Calcareous concretion from the upper unit as S4; the merus is about six times as long as wide, nearly of the Romualdo Formation, Fish Level, Santana Group, three-fourths of the carapace maximum length, somewhat middle to upper Albian, exposed at the south-eastern flank slender, nearly straight, and with weakly convex external of the Araripe Basin, near the city of Porteiras, Ceara, margins; no carpus, propodus or dactylus are known. As Brazil (Martins-Neto 1987, p. 407; Maisey 1991, p. 411; far as it can be recognized in the holotype, the P3 is very Maisey & Carvalho 1995,p.9). similar to P2 in shape and size; its coxa is about as long as Emended description. The holotype is a ventral cara- wide, wider towards basis; the basis-ischium is subtrian- pace of small size, subcircular in outline, approximately gular and short; the merus is about five times as long as as wide as long (10 mm width, 10 mm length), and wide, nearly straight, with external margins weakly con- with maximum width slightly anterior to carapace mid- vex, and narrow distally at articulation with carpus; the length. Its pterygostome is broad, vaulted, finely granu- carpus length is about one-third the length of merus and

Downloaded by [University of Alberta] at 22:49 10 January 2015 lated, and with a barely distinct blunt crest, and the two-thirds as wide as merus, narrower at the articulation cervical groove reaches the ventral carapace. The antero- with the merus, and wider at articulation with propodus, lateral margin is convex, slightly shorter than the postero- with smoothly convex external margins and nearly lateral margin, and apparently lacking spines; the straight internal margin; no propodus or dactylus are posterolateral margin is slightly convex, about as long as known. The P4 is partly preserved, with a reduced size anterolateral margin, and lacks visible spines. The buccal about half the length of P3; its merus is sub-cylindrical, cavity is elongated, at least three times as long as wide, about three times as long as wide and with margins nearly about half the carapace length, and nearly as long as tho- straight; the carpus is short and longer than wide with a racic sternum, as in other necrocarcinid-like terminals. sub-trapezoidal outline, about half as long but nearly as The thoracic sternum is narrow, about half the carapace wide as merus, narrower at the articulation with the length, and with the sternites more or less ﬂattened axi- merus, wider at articulation with propodus, and with its ally. Its episternites are directed posteriorly, and the exter- margins weakly convex; the propodus was not positively nal lobes of E4–E7 are sub-parallel to each other, lying recognized on the material studied, except for the sculpted oblique distally from the sternites (Figs 2A, B, 3A). The outline on the calcareous matrix (Figs 1A, B, 2A). In Mai- S1–S2 are unknown; but S3 is distinct ventrally, wider sey (1991, p. 432), however, a ﬂattened and sub-ovate than long, with a subrectangular outline and lateral mar- propodus seems to be present, about twice as long as car- gins somewhat straight, and slightly diverging anteriorly. pus, and nearly one-third wider than carpus. The P5 is the A puzzling Cretaceous frog crab from Brazil 159

smallest of all pereiopods, very reduced in size, and is wider than long as in Necrocarcinidae, Cenomanocarci- apparently carried dorsally; its merus is slender and small, nidae and Orithopsidae, but also as in several Palaeocor- sub-cylindrical in shape, about five times as long as wide; ystidae (Vega et al. 2007; Guinot et al. 2008; Vega et al. it is about one-fourth as long but about one-fifth as wide 2010; Karasawa et al. 2011; Van Bakel et al. 2012a). as P3, and just slightly longer than half the length of P4 but about one-fourth its width; the carpus, propodus and Phylogenetic analysis dactylus are unknown. In order to test the phylogenetic relationships of Araripe- carcinus with other brachyuran clades, two sets of analy- Remarks. Among necrocarcinids and their allies, only ses were performed. Analysis I was performed using the the genera Corazzatocarcinus Larghi, 2004, and Cenoma- original dataset of Karasawa et al. (2011), constituted by nocarcinus Van Straelen, 1936, have confirmed fossil rep- 37 taxa and 74 adult morphological characters, and scor- resentatives preserving the pereiopods, especially the ing Araripecarcinus following Karasawa et al. (2011) distal articles of P2 and P3, and complete P4 and P5 (Supplemental Table 1). Analysis II was performed using (Roger 1846; Feldmann et al. 1999; Neumann & Jagt an updated dataset for raninoidans after Karasawa et al. 2003; Larghi 2004; Vega et al. 2007; Guinot et al. 2008; (2011) and Van Bakel et al.(2012a) containing 14 taxa Vega et al. 2010) (Fig. 1). A specimen described as Ceno- and 44 adult morphological characters (Supplemental manocarcinus renfroae (Stenzel, 1945) by Vega et al. Tables 2, 3). Additional raninoidan taxa included in Anal- (2010) from the late Albian Simitı Formation of Colom- ysis II are Lyreididae Guinot, 1993, and Orithopsidae, bia, possesses similar P2 and P3 to those seen in speci- scored after Van Bakel et al. (2012a), plus the genus Ara- mens of C. vanstraeleni Stenzel 1945, while the P4 ripecarcinus, and the eubrachyuran family Portunidae, to resemble those seen on Corazzatocarcinus hadjoulae which Araripecarcinus was originally proposed to be (Roger, 1846) (Vega et al. 2010). Cenomanocarcinus ren- related with (Martins-Neto 1987). For Analysis II, out- froae, whose type series is known from the late Albian of group terminals were chosen and scored based on their Texas, was transferred by Van Bakel et al. (2012a) to phylogenetic positions after Karasawa et al. (2011),in Hasaracancer Jux 1971, the only other cenomanocarcinid order to explore the polarity of different plesiomorphic genus known to date from the Cretaceous (Osso-Morales and apomorphic traits seen in Raninoida with respect to et al. 2011; Van Bakel et al. 2012a). The Colombian spec- other ‘basal’ decapods. The rationale for scoring raninoi- imen of ‘C. renfroae’ was re-examined, and its affiliation dan taxa at the familial level is to convey the morphologi- with Cenomanocarcinidae corroborated based on the sub- cal diversity or disparity seen among raninoidans, and hexagonal carapace outline and the distinctive three longi- therefore be able to examine the combination of plesio- tudinal ridges, as accurately noted by Vega et al. (2010). morphic and apomorphic character states seen in Araripe- Nevertheless, given its poor carapace preservation, and carcinus. Ingroup terminals were chosen to test the since pereiopods in the Texas specimens of H. renfroae hypothesis of affiliation of Araripecarcinus with Portunoi- are unknown, direct comparison between the materials is dea (Eubrachyura). The datasets were produced or modi- problematic, and therefore its generic identity is unwar- fied in Mesquite (Maddison & Maddison 2011), and the ranted until new material becomes available. phylogenetic analyses were conducted in TNT 1.1 Despite the incomplete preservation of the pereiopods (Goloboff et al. 2008). All characters were unordered and in Araripecarcinus, the taxon shares with Cenomanocar- equally weighted. Branch supports were obtained in Mes-

Downloaded by [University of Alberta] at 22:49 10 January 2015 cinus, Corazzatocarcinus and the Albian cenomanocarci- quite. Traditional search for suboptimal trees included nid indet. from Colombia, slender P2 and P3 meri, similar 1000 replicates, and Implicit enumeration search was per- in shape and size and larger than those on P4 and P5, and formed without collapsing trees after the search. Both with the merus of P5 very reduced and carried in a sub- searches lead to the same topologies. Bootstrap and jack- dorsal plane (Fig. 1). The size of P4 is variable among knife values were obtained after 1000 replicates each. these taxa, from reduced in C. hadjoulae and the cenoma- Bremer support values for the traditional search were cal- nocarcinid indet., to moderately reduced in Araripecarci- culated under tree bisection reconnection (TBR), and nus, and slightly reduced in C. vanstraeleni. In extant retained trees suboptimal by 30 steps. Unknown character raninoid genera, shape and size of P4 may vary from states were scored as ‘?’, and inapplicable ones as ‘–’. noticeably reduced, nearly as much as P5, or just slightly The following abbreviations are used: TL, tree length; CI, shorter than P2–P3. Based on the illustration in Maisey consistency index; RI, retention index. (1991, p. 432), the apparently ﬂattened, slender and sub- Analysis I: tests the phylogenetic position of Araripe- ovate P4 propodus of Araripecarcinus is similar to Coraz- carcinus with respect to other podotreme and eubra- zatocarcinus, and less so to cenomanocarcinid indet, chyuran clades. It yielded nine equally most parsimonious while in Cenomanocarcinus it is broad, ﬂat, ovate, and trees, with TL ¼ 276 steps; CI ¼ 0.48; and RI ¼ 0.69 paddle-like (Feldmann et al. 1999; Vega et al. 2007, (Fig. 4). Given the incompleteness of Araripecarcinus, 2010; Guinot et al. 2008) (Fig. 1). In Araripecarcinus,A6 several of the characters in the dataset of Karasawa et al. 160 Javier Luque Downloaded by [University of Alberta] at 22:49 10 January 2015

Figure 4. Strict consensus of nine equally most parsimonious trees for main podotreme terminals and Araripecarcinus Martins-Neto, 1987, following the work of Karasawa et al. (2011). Tree length (TL) ¼ 276 steps; consistency index (CI) ¼ 0.48; retention index (RI) ¼ 0.69. Bremer support indicated above the branches, and bootstrap/jackknife values indicated below the branches, respectively. Terminal taxa indicated by y known only from fossil representatives. A puzzling Cretaceous frog crab from Brazil 161

(2011) cannot be scored for this terminal, resulting in a and are therefore included in Analysis II. In this analysis less resolved tree than the one obtained by the authors. In the topology is better resolved, and the polytomies dis- addition, the incompleteness of several other podotreme solved. The clade (Araripecarcinus (Camarocarcinus terminals (i.e. bucculentids, prosopids, tanidromitids, (Palaeocorystidae (Raninoidea)))) is united by the wide or glaessneropsids, konidromitids and lecythocarids) con- flattened P2 to P4, and is recovered as sister to (Orithopsi- tributes to the overall low branch support and ambiguity dae (Cenomanocarcinidae þ Necrocarcinidae)). However, for many clades. Despite this, in the strict consensus, Ara- this trait is homoplasious since Cenomanocarcinidae also ripecarcinus is recovered in a soft polytomy with all have wide or flattened P2 to P4. Araripecarcinus is recov- higher raninoidan taxa (Fig. 4). This clade is united by the ered as sister taxon to the clade (Camarocarcinidae (Palae- possession of an elongate buccal cavern, an mp3 lying in ocorystidae (Raninoidea))), which is united by the two planes, and flattened P2 to P4 (Karasawa et al. 2011; presence of an indistinct or faint cervical groove. This Van Bakel et al. 2012a). This group (Araripecarcinus þ character is polymorphic on Cenomanocarcinidae and raninoidan terminals) lies in a trichotomy with Etyoida Palaeocorystidae, as it is in the sister group to Raninoida. and the clade (Dakoticancroida (Cyclodorippoida þ The clade (Palaeocorystidae (Raninoidea)) is united by Eubrachyura)), providing further support to the hypothesis the shared elongate carapace, which is an apomorphic that Araripecarcinus might lie closer to Raninoida/Rani- condition among raninoidans. It is possible that Symethi- noidia than to any other podotreme or eubrachyuran clade. dae Goeke, 1981 constitutes a subfamily within Ranini- Analysis II: tests the phylogenetic position of Araripe- dae, rather than its sister taxon, as initially envisioned by carcinus with respect to higher Raninoida terminals. It Goeke (1981) (see Guinot 1993; Ahyong et al. 2007; Van yielded one most parsimonious tree, with TL ¼ 81 steps; Bakel et al. 2012a; Guinot et al. 2013; Karasawa et al. CI ¼ 0.85; and RI ¼ 0.87 (Fig. 5A). Since the work by 2014). Raninoidea is the clade stemming from the most Karasawa et al. (2011), some additional raninoidan fami- recent common ancestor for lyreidids, raninids, and syme- lies have been recognized (e.g. Van Bakel et al. 2012a), thids, all of them known from fossil and extant taxa. They Downloaded by [University of Alberta] at 22:49 10 January 2015

Figure 5. A, strict consensus of seven equally most parsimonious trees for Raninoida terminals, following the works of Karasawa et al. (2011) and Van Bakel et al. (2012a). Tree length (TL) ¼ 81 steps; consistency index (CI) ¼ 0.85; retention index (RI.) ¼ 0.87. Bremer support indicated above the branches, and bootstrap/jackknife values indicated below the branches. Terminal taxa indicated by y known only from fossil representatives. B, cladogram showing the three main clades constituting the monophyletic Raninoida (white oval). The necrocarcinid-like clade (dark grey oval), embracing those raninoidan terminals with usually broad, highly ornamented carapaces with deﬁned cervical and branchiocardiac grooves, and bearing branchial ridges or tubercles; i.e. Necrocarcinidae Forster,€ 1968, Cenomano- carcinidae Guinot et al., 2008 and Orithopsidae Schweitzer et al., 2003. Palaeocorystidae Lorenthey in Lorenthey & Beurlen, 1929 (grey oval), includes taxa with a somewhat ‘frog-like’ appearance, typically longer than wide, with carapaces varying from highly to poorly ornamented, and having well-deﬁned to faint cervical and branchiocardiac grooves. Raninoidea De Haan, 1839 (light grey oval) embraces those raninoidans with typical ‘frog-like’ longer carapaces, usually poorly ornamented to smooth, and with overall faint to incipient dorsal grooves. Camarocarcinidae Feldmann et al., 2007 and Araripecarcinus Martins-Neto, 1987 (dotted line) have dubious phylogenetic placement due their number of unknown character states, particularly Araripecarcinus. Main raninoidan apomorphies indicated by white bars and letters a to h. Terminal taxa indicated by a dagger (y) only known from fossil representatives. 162 Javier Luque

seem to share a long carapace, with straight to convex Tharrhias araripis Jordan & Branner, 1908; a presumed posterior margins, bearing narrow to reduced posterior plankton feeder (Maisey 1994;Maisey&Carvalho1995). sternites, and a presumed united spermatheca (Karasawa One larva (Fig. 6) seemingly lacks lateral spines, and bears et al. 2011). The palp of their mxp3 is carried in an inner short rostral and dorsal spines – the latter apparently bro- mesial position, and they have partially exposed pleurites ken, that are shorter than the carapace length. This is the associated to sternopleural extensions (Van Bakel et al. only fossil record of brachyuran protozoeal larva known to 2012a). Necrocarcinid-like taxa are confined to the fossil date (Maisey & Carvalho 1995; Guinot et al. 2013). In the record, ranging from the Early Cretaceous to the Palaeo- extant frog crab Ranina ranina (Linnaeus, 1758), instars I gene, and they differ from Raninoidea mainly, but not to VIII retain large rostral and dorsal spines, but lateral exclusively, in their broader carapaces, and the presence spines become faint to inconspicuous in late stages (Rice of branchial longitudinal ridges or rows of tubercles (Kar- &Ingle1977;Minagawa1990). Whether the fossil larva asawa et al. 2011; Van Bakel et al. 2012a). belong to a raninoidan, and particularly to Araripecarcinus, remains uncertain, but it clearly indicates that brachyurans were present in the shallow marine to brackish waters of Discussion the Araripe Basin during the Albian, and that they might have played an important role as food items at different Extant frog crabs are exclusively marine, ranging from ontogenetic stages (Maisey & Carvalho 1995). very shallow subtidal bottoms to nearly 1400 m depth As in extant raninoidans, the flattened articles of P2 to (Tucker 1995). Similarly, their fossils are known from P4 of Araripecarcinus might have assisted in burrowing, marine rocks worldwide, and no taxon has been reported and even occasionally swimming (Guinot et al. 2008, from freshwater settings. This suggests that Araripecarci- p. 688). The shape and proportions of P4 in raninoidans nus was a marine dweller, as hypothesized by Martins- can vary from a P4 slightly shorter than P2–P3 to nearly Neto (1987, p. 409). It was found in the same concretion as reduced as P5, and scoring these characters in further with the aspidorhynchid fish Vinctifer comptoni (Agassiz, phylogenetic analyses should reflect such variation in 1841), one of the most abundant fishes in the Romualdo sizes. The clades including Araripecarcinus and Camaro- Member, and considered to be a brackish to marine form carcinidae are poorly supported, and although both termi- (Martins-Neto 1987; Maisey 1991;Maisey&Carvalho nals were recovered as closer to Palaeocorystidae þ 1995). Based on palynomorphs, a mid–late Albian age has Raninoidea, it is likely that it is an artefact of their number been assigned to the Vinctifer-bearing horizons, and hence of unknown character states, being actually more closely to the Araripecarcinus specimen (Pons et al. 1990;Moody related to the clade formed by the necrocarcinid-like ter- &Maisey1994). Although Araripecarcinus is the only minals. Under either phylogenetic scenario, the superfam- adult brachyuran known from the Santana Group, and ily Palaeocorystoidea is paraphyletic, and suggests that therefore the Romualdo Formation, a few brachyuran zoea the plesiomorphic condition for raninoidans is to have larvae are known from stomach contents of the fish broader carapaces, indicating that the innovation of an Downloaded by [University of Alberta] at 22:49 10 January 2015

Figure 6. A, fossil brachyuran crab zoea AMNH 80038, fossil invertebrates, recovered as stomach contents from the fish Tharrhias araripis Jordan & Branner, 1908, AMNH FF 13680 (see Maisey 1994, fig. 10; Maisey & Carvalho 1995, fig. 4), from the Albian Romualdo Formation, late Early Cretaceous of the Araripe Basin, Brazil; B, close up of area shown in A. Abbreviations: Ds, dorsal spine; E, left compound eye bearing facets; Rs, rostral spine. A puzzling Cretaceous frog crab from Brazil 163

elongated carapace might have occurred only once in the plesiomorphic condition for raninoidans is to have broad evolutionary history of Raninoida, and is likely to have rather than elongate carapaces. However, due its large been present in the last common ancestor for Palaeocorys- number of unknown character states, its suprafamilial and tidae, Lyreididae and Raninidae (including Symethinae). familial placement are still uncertain, and based solely on Due to the incompleteness of Araripecarcinus, it is impos- the observed ventral traits, it is likely that Araripecarcinus sible for me to warrant its familial or suprafamilial place- was actually closer to the necrocarcinid-like stock than to ment, although the general sternal conﬁguration and Palaeocorystidae. The evolution of Cretaceous brachyur- carapace proportions are reminiscent of some necrocarci- ans is complex, with many body plans restricted to this nids. Camarocarcinidae was recovered as the sister taxon timeframe. Araripecarcinus might well belong to an to the clade (Palaeocorystidae (Raninoidea)), principally ancient, early-branching lineage of Aptian–Albian stem- due its lack of branchial ridges or rows of tubercles, as raninoidans endemic to northern South America. seen among necrocarcinid-like families. This might imply The clade containing the necrocarcinid-like taxa that: (1) the lack of branchial ornamentation is the plesio- include some of the oldest raninoidans known to date morphic condition for Raninoida, and such innovation (Hauterivian to late Aptian, 132 to 115 Ma), providing only evolved once in the most recent common ancestor further evidence that a more ‘crab-like’ body plan was the for (Orithopsidae (Cenomanocarcinidae þ Necrocarcini- ancestral condition for Raninoida and raninoidan-like dae)); or (2) that Camarocarcinidae, if assuming it is taxa. The key innovation of elongated carapaces, as seen closer to Orithopsidae þ (Cenomanocarcinidae þ Necro- in Palaeocorystidae, appears in the fossil record not long carcinidae) than to Palaeocorystidae þ Raninoidea, might after some ancient necrocarcinid-like taxa (late Aptian, have secondarily lost them (reversal), or never had them 115 Ma), followed by the oldest raninoids (mid Albian, (plesiomorphic). The evolution of Cretaceous brachyurans 108 Ma), and should have been present in the most is complex, with many body plans restricted to this time- recent common ancestor for Palaeocorystidae and Rani- frame. Araripecarcinus might well belong to an ancient, noidea. Under this scenario, the earliest palaeocorystids early-branching lineage of Early Cretaceous stem-raninoi- must have derived from a necrocarcinoid-like ancestor, dans endemic to Northern South America. but once they occupied a new morphospace, they marked Although frog crabs sensu lato are considered as a the evolutionary beginning of Raninoidea. Such transition monophyletic group, there is no agreement on whether from ‘crab-like’ to ‘frog-like’ carapaces could be related they constitute a section (Raninoida) alongside section to their burrowing lifestyle, raising the question if all Eubrachyura, or a subsection (Raninoidia) of section Podo- Raninoidans were burrowers, or if some ancient necrocar- tremata, within the Infraorder Brachyura (Ahyong et al. cinoid lineages were mostly epibenthic. 2007; Guinot et al. 2008;DeGraveet al. 2009; Schweitzer Phylogenetic analyses at the generic level are needed in et al. 2010; Karasawa et al. 2011; Ahyong et al. 2011;Van order to evaluate the position of Palaeocorystidae with Bakel et al. 2012a). This is a non-trivial issue, since each respect to Necrocarcinidae and allies and Raninoidea, rank underlies alternative hypotheses regarding the mono- helping to better resolve the raninoidan evolutionary tree phyly or paraphyly of Podotremata Guinot, 1977,and of life, and to gain a broader understanding on their relat- therefore the evolutionary relationships among the main edness by common ancestry throughout geological time. brachyuran lineages (Tavares 2003;Ahyonget al. 2007; De Grave et al. 2009; Karasawa et al. 2011). Since both

Downloaded by [University of Alberta] at 22:49 10 January 2015 suprafamilial ranks convey the same taxa, either taxon Acknowledgements would contain all the descendants from the most recent common ancestor for all frog crabs and allies. Although This work was supported by the Natural Science and raninoidan families tend to be distinctive from each other, Engineering Research Council of Canada Graduate Schol- their phylogenetic relationships at the generic level remain arship (NSERC CGS-D). My deepest thanks to Carlos Jar- unexplored (Karasawa et al. 2014). amillo (STRI), Daniele Guinot (MHNH), Kecia Kerr (McGill University), A. Richard Palmer (University of Alberta) and Hiroaki Karasawa (Mizunami Fossil Conclusions Museum, Japan) for intellectual support; to Paula Sucer- quia (Universidade de Sao Paulo) for providing photos Based on comparative anatomy and phylogenetic analy- and a cast of the holotype and sole specimen of Araripe- ses, Araripecarcinus is included within Raninoida, a carcinus ferreirai; to Rodney M. Feldmann (Kent State higher clade of brachyuran crabs that embraces the same University, USA) for providing photos of the cast of Ara- terminals included under the taxonomic ranks Raninoida ripecarcinus and the specimen of Cenomanocarcinus sp., and/or Raninoidia. Araripecarcinus, recovered as sister plus valuable comments that improved an early version of taxon to the clade uniting Camarocarcinidae, Palaeocorys- the manuscript; to Barry Van Bakel (Oertijdmuseum De tidae and Raninoidea, supports the hypothesis that the Groene Poort, Boxtel, The Netherlands) for thoughtful 164 Javier Luque

discussions and providing photos of Silvacarcinus;to Collins, J. S .H. & Smith, R. 1993. Ypresian (Lower Eocene) Roger Portell (FLMNH) and the Invertebrate Paleontol- crabs (Decapoda, Crustacea) from Belgium. Bulletin de ogy Division, Florida Museum of Natural History, Uni- l’Institut royal des Sciences naturelles de Belgique, Sciences de la Terre, 63, 261–270, pl. 261. versity of Florida, for the photo of Corazzatocarcinus; Dana, J. D. 1852. Crustacea. Pp. 1–1620 in United States and to John Maisey, Lorraine Meeker and Chester Tarka Exploring Expedition During the Years 1838, 1839, 1840, (AMNH, USA) for the photos of the Cretaceous bra- 1841, 1842 Under the Command of Charles Wilkes. U.S.N. chyuran larva preserved as stomach contents. I am very C. Sherman, Philadelphia. grateful to Carrie E. Schweitzer (Kent State University, Dawson, E. W. & Yaldwing, J. C. 2000. Description and eco- logical distribution of a new frog crab (Crustacea, Bra- USA), an anonymous reviewer, and the JSP editors for chyura, Raninidae) from Northern New Zealand waters, improving the quality of the manuscript. Partial funding with keys to Recent Raninid genera and Notosceles species. for this project was provided by an NSERC Canada Dis- Tuhinga, 11, 47–71. covery Grant A7245 to A. Richard Palmer. De Grave, S., Pentcheff, N. D., Ahyong, S. T., Chan, T. Y., Crandall, K. A., Dworschak, P. C., Felder, D. L., Feld- mann, R. M., Fransen, C. H. J. M., Goulding, L. Y. D., Lemaitre, R., Low, M. E. Y., Martin, J. W., Ng, P. K. L., Schweitzer, C. E., Tan, S. H., Tshudy, D. & Wetzer, R. Supplemental data 2009. A classification of Recent and fossil genera of decapod crustaceans. The Raffles Bulletin of Zoology Supplement, 21, 1–109. Supplementary material is available online DOI: 10.1080/ De Haan, W. 1830–1850. Crustacea. Pp. i-xxxi, 1–243, pls. 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