Bull. Natl. Mus. Nat. Sci., Ser. A, 44(2), pp. 41–50, May 22, 2018

Some Freshwater, Semi-terrestrial and Land (Crustacea, , Brachyura) from Ghana, West Africa

Masatsune Takeda1 and Hiromu Sugiyama2

1 Department of Zoology, National Museum of Nature and Science, 4–4–1 Amakubo, Tsukuba, Ibaraki 305–0005, Japan E-mail: [email protected] 2 Department of Parasitology, National Institute of Infectious Diseases, 1–23–1 Toyama, Shinjuku, Tokyo 162–8640, Japan E-mail: [email protected]

(Received 19 February 2018; accepted 28 March 2018)

Abstract Two freshwater crabs of the family Potamonautidae, Liberonautes chaperi (A. Milne– Edwards, 1887) and Potamonautes triangulus Bott, 1959, two semi-terrestrial crabs of the families and Sesarmidae, Goniopsis pelii (Herklots, 1851) and Guinearma huzardi (Desmarest, 1825), and a land of the family , Cardisoma armatum Herklots, 1851, are recorded from Ghana, West Africa. All the species are presented with brief taxonomical notes and some photographs for ready and steady identification. Key words: Freshwater crab, Semi-terrestrial crab, Land crab, Cardisoma armatum, Goniopsis pelii, Liberonautes chaperi, Guinearma huzardi, Potamonautes triangulus, Ghana, West Africa.

graphs of the closely related species. Introduction Some species of crabs dealt with in this paper In the collections of the National Museum of will serve the second intermediate hosts of lung Nature and Science, Tsukuba, are several speci- flukes not only for the primate and other wild mens of freshwater, semi-terrestrial and land mammals but also for the native people. crabs and three specimens of freshwater Macro- Although two representative West African Para- brachium prawn from Ghana, West Africa, col- gonimus species, P. uterobilateralis and P. afrika- lected by Mr. Sachio Yamamoto of JICA (Japan nus, both described by Voelker and Vogel (1965), International Corporation Agency) in 1990 and are unknown to date from Ghana, one of the sec- later donated by Prince Hitachino-miya Masahito ond intermediate hosts of them, Liberonautes for study. chaperi (A. Milne–Edwards, 1887), is included All of the crab specimens were identified with in the collection at hand. We, therefore, briefly the known species, with aid of monographic reviewed the literatures of the parasitological studies by Monod (1956), Manning and Holthuis studies on Paragonimus species and their host (1981) and Cumberlidge (1999), who dissolved crabs that were reported from the countries many nomenclatural problems and complex syn- neighboring Ghana for the forthcoming studies in onymies of the West African species. In spite of this country. The present report of freshwater, their contributions, however, the identification of semi-terrestrial and land crabs from Ghana will the West African freshwater crabs seems to be contribute to the study of lung flukes for ready still difficult for the researchers other than the and steady identification of the possible interme- decapologists dealing with the freshwater crabs, diate hosts, even if the numbers of the crab spe- because of lack of detailed figures or fine photo- cies are few. 42 M. Takeda and H. Sugiyama

In the following lines, the breadth and length as Sundanautes (Sundanautes) africanus chaperi. of the carapace are abbreviated as cb and cl, Finally, Cumberlidge (1985, p. 2703, fig. 1) respectively, and indicated in mm. All the speci- transferred this species to the genus Liberonautes mens are preserved in the collections of the Bott, 1955, with the detailed description and National Museum of Nature and Science, Tsu- comparison of the first male pleopod with those kuba (NSMT). of the congeneric species. Cumberlidge and Sachs (1989) made a key for the identification of four freshwater and semi-terrestrial crabs from Records of the Species Liberia including this species. Phylum ARTHROPODA: Subphylum According to Cumberlidge (1985) and Cum- CRUSTACEA: Class : berlidge and Sachs (1989), this species inhabits Order DECAPODA: Suborder PLEOCYEMATA: the rocky bottom of fast-flowing shallow water Infraorder BRACHYURA in Liberia, Côte d’Ivore and Ghana, and is never Superfamily Potamoidea found in the small streams or creeks. Family Potamonautidae Distribution. Côte d’Ivore, Ghana and Liberia. Genus Liberonautes Bott, 1955 Parasitological notes. Sachs and Cumber- Liberonautes chaperi (A. Milne–Edwards, 1887) lidge (1991a) found Liberonautes chaperi as the (Fig. 1) second intermediate host of Paragonimus utero- bilateralis in Liberia. Otherwise, according to Remarks. The specimens at hand are a Voelker and Sachs (1977), Sachs and Voelker mature female (NSMT–Cr 25808, Fig. 1A–D; cb (1982), Sachs and Cumberlidge (1991b), and including lateral teeth 67.3×cl 45.2 mm) and an Cumberlidge (1999), the following three of eight immature female (NSMT–Cr 25809, Fig. 1E–F; Liberonautes species, L. latidactylus (De Man), cb 48.2×cl 32.5 mm). This species attains to L. nanoides Cumberlidge and Sachs, and L. palu- large size, as one of the females examined is still dicolis Cumberlidge and Sachs, have also been immature in spite of its considerable size. This shown to harbor the metacercariae of Paragoni- species is most characterized by the presence of mus uterobilateralis [Japanese name: Fohgeru- the intermediate spiniform or rather tubercular hai-kyuchu] or P. afrikanus [Japanese name: Afu- tooth between the external orbital and epibran- rika-hai-kyuchu], both of which were described chial teeth, the imperfect postfrontal crest not by Voelker and Vogel (1965). reaching the epibranchial tooth at each lateral According to Aka et al. (2008) who summa- side, and the presence of three to six, mostly five, rized the human paragonimiasis in Africa, Sun- spiniform teeth behind the epibranchial tooth at danonautes africanus (A. Milne–Edwards) is the the anterolateral carapace margin. Among these main carrier of metasercariae of Paragonimus characters, the spiniform teeth at each anterolat- uterobilateralis in Cameroon and Nigeria, and eral carapace margin enable to this species quite two species of the same genus, S. aubryi (H. distinctive among the eight congeneric species of Milne Edwards) and S. granulatus (Balss), are of Liberonautes, as shown in the key made by Cum- little importance, being the hosts of metacercariae berlidge (1985), with the spiny river crab as the of P. uterobilateralis or P. africanus. In addition common name in Liberia. to the two species, Aka et al. (2008) listed S. pelii This species was originally referred to the (Herklots) as carrier of metacercariae, but as seen genus Parathelphusa H. Milne Edwards, 1853, in Ng et al. (2008), S. pelii is now taxonomically by A. Milne–Edwards (1887, p. 144, pl. 8 fig. 4), known as a synonym of S. aubryi. In Liberia the and then recorded by Rathbun (1905, p. 202, pl. unique host crab is Liberonautes latidactylus 12 fig. 6) under the name of Potamon (Parathel- which is infected only with P. uterobilateralis. It phusa) chaperi, and later by Bott (1955, p. 298) is noted here that the occurrence of unidentified Freshwater, Semi-terrestrial and Land Crabs from Ghana 43

Fig. 1. Liberonautes chaperi (A. Milne–Edwards, 1887). A–D: Female (NSMT–Cr 25808; cb including lateral teeth 67.3×cl 45.2 mm). E–F: Young female (NSMT–Cr 25809; cb 48.2×cl 32.5 mm).

metacercariae in marginatus (A. berti. Otherwise, absence of paragonimiasis in Milne–Edwards) from Benin reported by Aka et Ghana is remarkable, but the fact is yet to be al. (2008) is not always reliable, because the crab measured and further investigated. In the present is marine swimming crab () living in collection are two specimens (Fig. 1) identified as shallow waters. Later, Bayssade–Dufour et al. Liberonautes chaperi, but no specimen referable (2014, 2015) showed S. africanus from Camer- to the congeneric species, L. latidactylus, which oon as the second intermediate host of two new was originally described from Ghana and occurs lung fluke species, P. gondwanensis and P. ker- in the West African rain forest area from Ghana to 44 M. Takeda and H. Sugiyama northwards to Senegal. Occurrence of paragoni- margins. The postfrontal crest is strong, com- miasis in Ghana seems to be reasonable as far as plete, transverse, reaching the epibranchial tooth the present knowledge concerned. to each anterolateral carapace margin. The exter- nal orbital angle is triangular, directed forward with subacute tip. The ebibranchial tooth is simi- Genus Potamonautes MacLeay, 1838 lar to the external orbital tooth in shape, but Potamonautes triangulus Bott, 1959 smaller. The anterolateral carapace margin is reg- (Fig. 2) ularly convex, narrowly ridged and granulated Remarks. The specimens examined are two throughout the length. The posterior end of the juvenile females (NSMT–Cr 25810, Fig. 2A–B, marginal ridge is weakly directed dorsally. The cb 33.4×cl 24.1 mm; NSMT–Cr 25811, Fig. carapace postero-dorsal surface is weakly 2C–D, cb 33.5×cl 23.9 mm), representing a typi- depressed and ornamented with some weak, cal form of Potamonautes in the flattened and oblique ridges. The abdomen of the female speci- ovate carapace, without intervening tooth men at hand is still not developed and similar to between the external and epibranchial teeth. It is male abdomen (Fig. 2B). identified with P. triangulus described by Bott According to Cumberlidge (1999), the West (1959, p. 1002) and redescribed by Cumberlidge African Potamonautes are represented by four (1999, p. 135). The carapace is nearly smooth, species, P. ecorssei (Marchand, 1902), P. senega- only with small granules along the anterolateral lensis Bott, 1970, P. reidi Cumberlidge, 1999,

Fig. 2. Potamonautes triangulus Bott, 1959. A–B: Juvenile female (NSMT–Cr 25810; cb 33.4×cl 23.9 mm). C–D: Juvenile female (NSMT–Cr 25811; cb 33.5×cl 23.9 mm). Freshwater, Semi-terrestrial and Land Crabs from Ghana 45 and this species. Of these, P. ecorssei and this and records of the specimens are referred to species are known from Ghana, but P. ecorssei is Monod (1956) as G. cluenlata and Manning and readily distinguished from this species by the Holthuis (1981) as G. pelii. distinctly quadrate carapace shape, and the sharp Distribution. West African coast from Sene- external orbital and epibranchial teeth. gal to Angola. Distribution. Endemic to Ghana, living in the rivers. Family Sesarmidae Genus Guinearma Shahdadi and Schubart, 2017 Superfamily Guinearma huzardi (Desmarest, 1825) Family Grapsidae (Fig. 3A–D) Genus Goniopsis De Haan, 1833 Goniopsis pelii (Herklots, 1851) Remarks. A male (NSMT–Cr 25813, Fig. 3A–D, cb 28.2×cl 23.5 mm), and a female (Fig. 3E–F) (NSMT–Cr 25814, cb 30.0×cl 25.2 mm) at hand Remarks. A female (NSMT–Cr 25812, cb agree well with the line drawing of 29.3×cl ca. 23.2 mm) at hand is somewhat dam- (Chiromantes) huzardi (Desmarest) given by aged for the main part of the carapace, but agrees Monod (1956, fig. 593). However, the subgenus well with the line drawing of a male of Goniop- Chiromantes Gistel, 1848, a replacement name sis cluenlata (Latreille, 1803) by Monod (1956, for preoccupied Pachysoma De Haan, 1833, is a fig. 564). Manning and Holthuis (1981, p. 227) senior objective synonym of Holometopus H. dissolved some nomenclatural problems as for Milne Edwards, 1853, as definitely shown by the priority and synonymy, and indicated that the Holthuis (1977, pp. 170–171), and the subgenus correct name of the West African Goniopsis spe- Chiromantes used by Serène and Soh (1970) and cies is not G. cluenlata (Latreille), but G. pelii most of the recent authors should be known as (Herklots), with detailed comparison of two spe- the genus Perisesarma De Man, 1895. Since cies from South America and Africa. then, Sesarma (Chiromantes) huzardi is known The carapace (Fig. 3E) is quadrate and slightly as S. (Perisesarma) huzardi dealt with by Man- wider than long, with the lateral margins weakly ning and Holthuis (1981, p. 245) or Perisesarma converging posteriorly; the dorsal surface is not huzardi listed by Ng et al. (2008, p. 222). convex, divided into regions by shallow furrows, Ng et al. (2008) listed 21 definite and 2 sus- with some transverse linear furrows at the frontal pended species in the genus Perisesarma, and gastric regions, and several at the branchial although P. kammermani (De Man, 1883) should regions. A small notch is just behind the external be included in the suspended species group from orbital angle. The female specimen at hand lacks West Africa together with P. huzardi (Desmarest, the left cheliped. The right chela (Fig. 3F) is 1825) and P. alberti Rathbun, 1921. Afterwards moderate in size, with the smooth palm, and both Davie (2010) and Shahdadi et al. (2017) fingers are armed with sharp granules along mar- described each a new species from Western Aus- gins. The ambulatory legs are stout and tralia and Vietnam, respectively. In the descrip- depressed; the meri are more or less foliate, tion of the new species from Western Australia, many linear transverse furrows on each dorsal Davie (2010) noted that three West African spe- surface, with small subterminal notch at each cies sharing a number of unique apomorphies are anterior margin. certainly need to be transferred to the genus dis- Manning and Holthuis (1981) summarized the tinct from the Indo–West Pacific species. Very habit and habitat of this species. Most of the recently, Shahdadi and Schubart (2017) thor- records in the literature reported on them living oughly revised the genus Perisesarma based not in the muddy bottom of mangroves. Literatures only by the morphological characters but also the 46 M. Takeda and H. Sugiyama

Fig. 3. Guinearma huzardi (Desmarest, 1825). A–D: Male (NSMT–Cr 25813; cb 28.2×cl 23.5 mm). Goniopsis pelii (Herklots, 1851). E–F: Female (NSMT–Cr 25812; cb 29.3×cl ca. 23.2 mm). molecular analysis. As a result, 1) the genus Peri- Man, 1895. The most recently described Peri- sesarma is restricted only to the type species, sesarma tuerykayi Shahdadi, Davie and Schu- Sesarma dussumieri H. Milne Edwards, 1853, 2) bart, 2017 is reasonably referred to Parasesarma. Perisesarma fasciatum (Lanchester, 1900) was The carapace (Fig. 3A) is distinctly quadrate, designated as the type species of a new genus with areolated and roughened dorsal surface cov- Fasciarma, 3) three West African species were ered with many but isolated patches of short generically separated from the Indo–West Pacific setae. The frontal part of the carapace is almost species under the new name Guinearum, and the perpendicularly deflexed, and in the frontal view other 19 Indo–West Pacific Perisesarma species (Fig. 3C), four prominent lobes occupy the space were transferred to the genus Parasesarma De between the orbits of both sides. The lateral mar- Freshwater, Semi-terrestrial and Land Crabs from Ghana 47 gins of the carapace are nearly longitudinal, with rower in C. weileri. a distinct notch behind each external orbital The specimen at hand is a male (NSMT–Cr angle and a small interruption further posteriorly; 25815, cb 45.0×cl 33.5 mm) and safely identi- the tips of the external orbital and lateral teeth fied with Cardisoma armatum which represents thus formed are pointed and directed forward and the typical Cardisoma shape of the carapace, obliquely outward, respectively. The male cheli- chelipeds and ambulatory legs like the Indo– peds are heavy and slightly different in size. The West Pacific species. It may attain larger size of upper surface of the palm is armed with about 10 cm or more in carapace breadth as recorded by four oblique subparallel granulated ridges. The Rathbun (1921, p. 262). The carapace (Fig. 4A) upper surface of the movable finger is orna- is smooth, vaulted at both branchial regions, and mented with about 15 blunt stridulating granules strongly convergent posteriorly; mesogastric, each crossed by fine impressed lines. cardiac and intestinal regions are marked with The old literature, records of many specimens linear furrows, and also the bifurcation of the from Senegal to Angola, and line drawing of a beginning of the gastric region is distinct at the male are referred to Monod (1956, p. 437, fig. postofrontal region. The outer half of the supra- 593) as Sesarma (Chiromantes) huzardi, and the orbital margin is narrowly raised, with the exter- description and photographs are referred to Rath- nal margin being sharply anguler. The branchial bun (1918, p. 287, pl. 75; 1921, p. 446, pl. 41, pl. margin is convex and fringed with a linear ridge, 42 fig. 2) as S. (C.) africanum H Milne Edwards, with a small notch just behind the external orbital 1837. Manning and Holthuis (1981, p. 245) also angle. The posterolateral margin of the carapace recorded many specimens from wide areas along is shallowly concave dorsally, with a linear ridge the West African coast from Senegal to Angola from the anterolateral branchial margin and also including Ghana. with some oblique, linear ridges. The pterygosto- Manning and Holthuis (1981) recorded that mial region (Fig. 4D) is covered with short setae, this species is found in mangroves, salt marshes, with the infraorbital margin being entire and tidal rice lands and mouths of rivers. As far almost transverse for its most part. Both cheli- known from the literature, the habit and habitat peds (Fig. 4B) are quite unequal in the size and are quite similar to those of the Indo-West Pacific shape; in the right smaller chela both fingers are Perisesarma species known as Parasesarma at nearly straight, with small teeth throughout the present. cutting edges, leaving no space between both fin- Distribution. West African coast from Sene- gers; the left larger cheliped (Fig. 4C) is heavy, gal to Angola. and the palm is smooth for its most outer surface, but heavy granulated along the lower margin; the immovable finger is armed with a strong tooth Family Gecarcinidae just in the middle of the cutting edge, and the Genus Cardisoma Latreille, 1828 movable finger with a similar tooth at the basal Cardisoma armatum Herklots, 1851 one third of the cutting edge, leaving a space (Fig. 4) interrupted at the teeth. The male abdomen (Fig. Remarks. The land crab family Gecarcinidae 4E) is narrow, the penultimate segment being from the eastern Atlantic coast is represented thrice as long as the telson. The male first pleo- only by two species of two genera, Cardisoma pod (Fig. 4F) is short and hairy, with the terminal armatum Herklots, 1851 and Gecarcinus weileri horny tip directed dorsally and the large flap (Sendler, 1912). Both species are distinctive at against the terminal tip. the first glance in the general appearance of the The full descriptions, complete synonymies, carapace; the front-orbital border is wider than photographs of the specimens and line drawings 1/2 carapace breadth in C. armatum and nar- of the first male pleopod were given by Rathbun 48 M. Takeda and H. Sugiyama

Fig. 4. Cardisoma armatum Herklots, 1851. A–F: Male (NSMT–Cr 25815; cb 45.0 ×cl 33.5 mm).

(1921, p. 456, fig. 21, pl. 48 figs. 1–2) and Manning and Holthuis (1981). Türkay (1973, p. 86, figs. 1, 3, 7–8), the fine line Distribution. Cape Verde Islands, and West drawing of a male by Monod (1956, fig. 618), African coast from Senegal to Angola. and many specimens from the West African countries were recorded by Monod (1956) and Freshwater, Semi-terrestrial and Land Crabs from Ghana 49

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