Pseudohelice latreillii (H. Milne Edwards, 1837 )

Hsu, Jhih-Wei, Shih, Hsi-Te & Innocenti, Gianna, 2022, A review of the mud crab genus Pseudohelice Sakai, Türkay & Yang, 2006 (Crustacea: Brachyura: Varunidae), with redescription of Cyclograpsus latreillii H. Milne Edwards, 1837, from the western Indian Ocean, Raffles Bulletin of Zoology 70, pp. 94-107 : 100-104

Pseudohelice latreillii (H. Milne Edwards, 1837)

( Fig. 3 )

Cyclograpsus latreillii H. Milne Edwards, 1837: 80 ( Mauritius) .

Helice latreilli —H. Milne Edwards, 1853: 190 (part) ( Mauritius).

Pseudohelice subquadrata — Sakai et al., 2006: 37 (part) ( Egypt, Kenya, Mauritius, Seychelles; “ paralectotype ” of C. latreillii ); Naderloo, 2017: 360, fig. 32.4 ( Socotra).

? Pseudohelice subquadrata — Hywel-Davies, 1994 ( Oman); Naderloo et al., 2015: 408 (list) ( Oman).

Material examined. Neotype male (16.6 × 14.0 mm) ( MZUF 4991 ), Petit Gravier , Rodrigues I., Mauritius, coll.

M. Vannini, 9 July 1989; leg. M. Vannini. Egypt: 1 female (14.8 × 12.3 mm) ( MZUF 3790 ), Nabq-El Arwashie , Sinai, coll. S. Barbaresi, A. Conti, S. Fratini & G. Innocenti, 15 October 2004 . Kenya: 1 female (17.5 × 14.8 mm) ( MZUF 4985 ), Mida Creek , coll. M. Vannini, March 1999 ; 1 female (17.8 × 15.1 mm) ( MZUF 4993 ), Mida Creek , coll. M. Vannini, September 1998 ; 1 female (17.4 × 14.8 mm) ( MZUF 4987 ), Gazi , coll. S. Cannicci, August 1998 . Seychelles: 2 females (13.9 × 11.8, 14.6 × 12.2 mm) ( MZUF 2935 ), Mahé, Port Launay , coll. S. Fratini, December 2005 ; 2 males (15.8 × 13.6, 18.7 × 16.3 mm) ( MZUF 4989 ), Ile Moustiques, Aldabra , coll. M. Vannini, March 1979 . Mauritius: 1 female (21.5 × 16.1 mm) (MNHN-IU-2000-3468 = MNHN-B3468 ) ; 1 female (17.5 × 14.5 mm) (MNHN-IU-2013-14768 = MNHN-B3468 ) ; 6 males (15.3 × 13.0, 18.4 × 16.6, 18.7 × 15.4, 19.1 × 16.6, 19.4 × 16.5, 19.8 × 16.9 mm), 2 females (16.3 × 14.0, 19.5 × 16.4 mm) (MNHN-IU-2013-14769 = MNHN-B12096 ) , 4 males (14.0 × 12.2, 15.5 × 13.3, 16.5 × 14.4, 18.4 × 16.0 mm), 7 females (14.2 × 12.4, 15.9 × 13.4, 16.8 × 14.2, 16.9 × 13.7, 18.0 × 15.5, 19.3 × 15.9, 19.3 × 16.0 mm) (MNHN-IU-2013-14770 = MNHN-B12095 ), coll. M. Carié, 1913 (identified by M. Türkay in 1983 as Helice leachii Hess, 1865 ) ; 1 male (15.9 × 13.4 mm) ( MZUF 4991 ), Petit Gravier , Rodrigues I., coll. M. Vannini, 9 July 1989 ; 1 male (18.5 × 16.0 mm) ( MZUF 4999 ), Baie Aux Huitres , Rodrigues I., coll. M. Vannini, 8 July 1989 ; 4 males (14.8 × 12.3, 16.5 × 14.0, 17.0 × 14.7, 17.1 × 14.2 mm), 3 females (11.1 × 9.5, 14.2 × 12.2, 16.5 × 14.0 mm) ( MZUF 4994 ), Poste Lafayette , coll. M. Vannini, 4 July 1989 ; 3 females (7.7 × 6.6, 9.8 × 8.2, 17.3 × 14.2 mm) ( MZUF 4997 ), Melville , coll. M. Vannini, 1 July 1989 .

Description. Carapace ( Fig. 3A, C ) quadrate, slightly broader than long, 1.18 times as broad as long; surface convex, weakly punctate, granulated, with noticeable groove between epigastric regions. Frontal margin slightly concave. Anterolateral margins with 3 teeth including orbital tooth; last tooth weak, sometimes indistinct. Posterolateral margins almost parallel, not divergent posteriorly, moderately sloping outwards; lateral and posterolateral margins regularly furnished with short, soft setae.

Infraorbital ridge ( Fig. 3E ) in male heteromorphic, mesial part with several small rounded tubercles, followed by several large, elongated and less convex tubercles, lateral part with 1 largest and very convex rounded tubercle, and 2 large rounded and convex tubercles; 2 forms in female, form I: mesial part with several small rounded tubercles, followed by well-spaced several small, isomorphically rounded tubercles in lateral part ( Fig. 3F ); form II: mesial part with several larger rounded tubercles, followed by well-spaced several small, heteromorphic, elongated and less convex tubercles, lateral part with 1 largest and 2–5 larger convex tubercles ( Fig. 3G ). Chelipeds ( Fig. 3D ) with palm bulky, almost glabrous; usually unequal in adult male and equal in adult female. Ambulatory legs ( Fig. 3A, B ) slender, anterior margins of merus, carpus, and propodus covered with dense short setae; posterior margins with sparse short setae. Male G1 ( Fig. 3H–K ) slender, weakly tapering, slightly curved towards lateral end, with a pointed tip, distal part slightly V-shaped, bilobed; female vulvae ( Fig. 3L–M ) with an elongated semi-circular sternal vulvar cover; sunken on inner part.

Size. Largest male CW 18.7 mm (MZUF 4989), largest female CW 17.5 mm (MZUF 4985).

Distribution. Oman (?), Yemen ( Socotra I.), Egypt (Red Sea), Kenya, Seychelles, Mauritius, and Rodrigues I. ( Sakai et al., 2006; Naderloo et al., 2015; this study; Fig. 4 ).

Remarks. After examining a series of specimens, identified as “ P. subquadrata ”, collected from Mauritius, Kenya, and the Red Sea, we found they have a suite of reliable characters different from those of Pseudohelice subquadrata from the West Pacific. The challenge was to decide which name should be applied to this second Pseudohelice species, or if it should be described as new. We here argue that the name Cyclograpsus latreillii H. Milne Edwards, 1837 should be applied to it.

In the collection of MNHN, three of H. Milne Edwards’ specimens of Cyclograpsus latreillii (2 dry and 1 regenerated in alcohol) from “Ile de France ” (= Mauritius) have been found. The dry male specimen (MNHN-IU-2000-4647 = MNHN-B4647), with CW and CL of 33.7 × 27.2 mm is the lectotype of C. latreillii selected and identified as Helice tridens by Sakai et al. (2006: fig. 34). Sakai et al. (2006: 24) cited the measurements of the lectotype as 35.0 × 27.0 mm but in their caption for the photograph of the specimen, it was stated to be 35.0 × 28.0 mm ( Sakai et al., 2006: 25); nevertheless, these are close enough to the present measurements. Sakai et al. (2006) commented that since Helice tridens is only known from East Asia, their lectotype of Cyclograpsus latreillii must have been incorrectly labelled as being from Mauritius. Another dry female (MNHN- IU-2000-3468 = MNHN-B3468) (21.5 × 16.1 mm) is the paralectotype of C. latreillii selected by Sakai et al. (2006) and was referred to Pseudohelice subquadrata by Sakai et al. (2006). A third female specimen (MNHN-IU-2013-14768 = MNHN-B3468) (ca. 17.5 × 14.5 mm), regenerated in alcohol and labelled as a syntype, was not examined by Sakai et al. (2006), but was identified as “ Pseudohelice leachi ” by M. Türkay in 1983 (not published); this taxon is now regarded as a junior synonym of Pseudohelice subquadrata . Photographs of both female specimens were examined, and the structure of their infraorbital ridges agree with the material from eastern Africa, i.e., the second species of Pseudohelice . The dry specimen (MNHN-IU-2000-3468) has the “form II” type of infraorbital ridge while the wet-preserved female (MNHN- IU-2013-14768) has “form I” type (see later).

Although these three MNHN specimens are labelled as syntypes, and Sakai et al. (2006) accepted their authenticity, selecting a lectotype in the process, we do not believe they are actually types. There are serious discrepancies in the description and measurements provided by H. Milne Edwards (1837) when compared to the three specimens. In his brief description of C. latreillii, H. Milne Edwards (1837: 80) wrote “Carapace presque quadrilatère, très-élevée et armée de trois dents de chaque côté.” [Carapace almost quadrilateral, very high, and armed with three teeth on each side]. Of the three supposed syntypes, only the two females of Parahelice subquadrata (MNHN-IU-2000-3468, 21.5 × 16.1 mm; MNHN-IU-2013-14768, ca. 17.5 × 14.5 mm), have three anterolateral teeth. The dry male of Helice tridens (MNHN-IU-2000-4647, 33.7 × 27.2 mm) has four anterolateral teeth and even though the last one is small, it is still visible and H. Milne Edwards is unlikely to have missed this tooth in his account. Henri Milne Edwards (1837: 80) also clearly stated that the CL of the species was “4 lignes” (ca. 9 mm). This size is substantially smaller than any of the three supposed syntypes. While H. Milne Edwards (1837) did not state how many specimens he had on hand, and it is possible that the 9 mm CL specimen H. Milne Edwards listed is now lost, it is still most unlikely that he would cite the smallest specimen he had in the publication and not measure the largest one! While Pseudohelice subquadrata has three anterolateral teeth, both the supposed syntypes are much larger than 9 mm CL; and the even larger supposed lectotype has four anterolateral teeth instead. Many years later, H. Milne Edwards (1853: 190) redescribed the taxon (as Helice latreilli ), stating that it was a large species with four anterolateral teeth, the last being rudimentary; but he did not state how many specimens he had or provide sizes. The available evidence thus indicates that the three supposed specimens of Cyclograpsus latreillii now in MNHN are not syntypes, having been mislabelled in the past, and that the 9 mm CL specimen listed by H. Milne Edwards is now lost. Between 1837 when he named the species, and 1853 when he redescribed it, H. Milne Edwards probably obtained more specimens of this species, but these cannot be treated as types. This additional non-type material probably included the large male selected as the lectotype by Sakai et al. (2006), and someone incorrectly labelled the specimens as types.

As a result, the designation of lectotype and paralectotype by Sakai et al. (2006) is suggested to be invalid (Article 74.2, ICZN, 1999). The original description by H. Milne Edwards (1837) unfortunately is too brief and does not allow us to determine if the species is Pseudohelice or Parahelice as both genera occur in eastern Africa ( Sakai et al., 2006). Sakai et al. (2006) reports “ Pseudohelice subquadrata ” from eastern Africa (which includes our present material) and described Parahelice balssi ( Sakai, Türkay & Yang, 2006) from South Africa. Cyclograpsus latreillii can be either or neither taxon, and since the type(s) is here regarded as lost, the only objective way to resolve its identity is to select a neotype for the species. The two old non-type MNHN specimens (MNHN-IU-2000-3468, MNHN-IU-2013-14768) listed above are Pseudohelice latreillii as discussed, but both are not in good condition, and a male specimen is preferable as a neotype having more characters. In addition, considering the wrong provenance of the third specimen (the incorrectly designated lectotype male), we are not sure if they originated from Mauritius. Since Parahelice balssi is already described in detail and from South Africa (not yet known from Mauritius), for the purpose of nomenclatural stability, it is prudent to select a male specimen of the second species of Pseudohelice from eastern Africa (which is known from Mauritius) to be the neotype. Among material from the WIO, small specimens with ca. 9 mm CL (MZUF 4994 and MZUF 4997) also agree with the description of H. Milne Edwards (1837) in the shape of the carapace and the number of anterolateral margin teeth. We here select a male (16.6 × 14.0 mm) (MZUF 4991) collected from Rodrigues I., Mauritius as the neotype of Cyclograpsus latreillii H. Milne Edwards, 1837 .

Morphologically, Pseudohelice latreillii is similar to P. subquadrata and the two can be easily confused. In both sexes of adults, no obvious difference was found in the characters of dorsal carapace, chelae, and ambulatory legs, but they can be distinguished by the forms of their infraorbital ridges, G1s, and vulvae ( Table 2). For the males of Pseudohelice latreillii , the largest tubercle of the lateral part of the infraorbital ridges is rounded ( Fig. 3E ) (vs. elliptical in P. subquadrata ; Fig. 1E ; Sakai et al., 2006: fig. 57); and the G1 is slenderer, the distal part is tubular, the chitinous structure at the top is relatively wider, shorter and thicker, and the tip is blunter ( Fig. 3H–K ) (vs. the G1 is stouter and blunter, the distal part is slightly flatter; the chitinous structure at the top is relatively smaller and thinner, and the tip is pointed in P. subquadrata ; Fig. 1G–J ; Sakai et al., 2006: fig. 53).

Two forms of infraorbital ridges have been observed in female P. latreillii . As both forms can be found in our specimens with similar sizes and/or from the same region, for now we treat them as intraspecific variations. Form I in P. latreillii is distinct from that in P. subquadrata , but the form II of P. latreillii is more similar to that in P. subquadrata ( Table 2). Among the specimens of P. latreillii , form I ( Fig. 3F ) is more common, with the infraorbital ridge consisting of several small rounded tubercles in mesial part, and well-spaced several small isomorphically rounded tubercles in lateral part. Form II ( Fig. 3G ) is less common, the infraorbital ridge consisting of several well-spaced and larger rounded tubercles in the mesial part, followed by well-spaced several small heteromorphic elongated and less convex tubercles, the lateral part with 1 largest and 2–5 larger convex tubercles (vs. several dense small tubercles in the mesial part, followed by closely spaced several larger and less convex tubercles, the lateral part with 1 largest and 2–5 larger convex tubercles in P. subquadrata ; Fig. 1F ; Sakai et al., 2006: fig. 58). In addition, the sternal vulvar cover is relatively but consistently shorter in P. latreillii ( Fig. 3L–M ) (vs. longer in P. subquadrata ; Fig. 1K ).

An additional note on Pseudohelice subquadrata s. str. is necessary. Sakai et al. (2006) showed that Helice leachii Hess, 1865 is a junior synonym of Pseudohelice subquadrata s. str. but noted that Hess’ specimens could not be found. Hess (1865: 153) stated that his material was from “Sydney” but it is well known that they could also have come from anywhere else in the South Pacific. Ng (2012) and Ng et al. (2020) discussed the problem at length and searched for Hess’ material in Germany and Sweden. We are now confident that the types of Helice leachii are no longer extant. Although we are here describing a second species of Pseudohelice from some distance away in the WIO, it is in the interests of stability that the identity of Helice leachii Hess, 1865 must be fixed through the appropriate designation of a neotype that will keep it as a synonym of Pseudohelice subquadrata ( Dana, 1851) s. str., and not potentially cause problems with other taxa. As such, we here select the specimen designated as the neotype of Chasmagnathus subquadratus Dana, 1851 (a male, 18.2 × 16.0 mm) from Salilor’s Bay, Sydney, New South Wales, Australia (Queensland Museum catalogue number QM W 2269) to be the simultaneous neotype of Helice leachii Hess, 1865 . As a result, both names now become objective synonyms.

Molecular analyses. The COI sequences analysed include 13 specimens of Pseudohelice subquadrata from Taiwan, Guam, Indonesia (Bali), and eastern Australia, and 11 specimens of P. latreillii from eastern Africa ( Table 1). The pairwise nucleotide divergences of K2P distances and bp differences among haplotypes of the two species are shown in Table 3. The intraspecific nucleotide divergences (and bp differences) of P. subquadrata and P. latreillii are ≤ 1.4% (≤ 9 bp) and ≤ 1.9% (≤ 12 bp), respectively. The interspecific divergences are 3.3%–5.1% (21–32 bp).

The phylogenetic tree ( Fig. 5 ) based on COI shows that the specimens from the western Pacific form a distinct clade, sister to another clade with the specimens from eastern Africa. The nucleotide divergences and the phylogeny both support the recognition of two distinct species.

Figures

Fig. 3. Pseudohelice latreillii (H. Milne Edwards, 1837). A–D, H–K, male (16.6 × 14.0 mm, neotype, MZUF 4991); F, L, female (17.3 × 14.2 mm, MZUF 4997); G, M, female (14.6 × 12.2 mm, MZUF 2935). A, dorsal view of male; B, ventral view of male; C, carapace; D, outer view of male left cheliped; E, left male infraorbital ridge; F, G, left female infraorbital ridge (F, form I; G, form II); H, J, dorsal view of right G1; I, K, ventral view of right G1; L, M, right vulva.

Fig. 4. The geographical distribution of Pseudohelice subquadrata (red dotted line) and P. latreillii (blue dotted line). The red solid circles are collection sites of specimens used in this study. The range was established by the additional records from references (see synonym lists for each species). The numbers correspond to the locality of specimens in Table 1. Empty triangles and circles mean the additional records from other references (see list of synonymies). “*” indicates the type locality.

Fig. 1. Pseudohelice subquadrata (Dana, 1851). A, B, E, G–J, male (19.2 × 17.1 mm, QM W19922); C, D, F, K, female (20.9 × 18.3 mm, QM W19922); A–D in preservative. A, dorsal view of male; B, ventral view of male; C, dorsal view of female; D, ventral view of female; E, left male infraorbital ridge; F, left female infraorbital ridge; G, I, dorsal view of left G1 (horizontally flipped); H, J, ventral view of left G1 (horizontally flipped for comparison with the right G1s of other specimens); K, right vulva.

Fig. 5. Bayesian inference (BI) tree for Pseudohelice subquadrata and P. latreillii, and the outgroups, based on the cytochrome c oxidase subunit I (COI) gene. Probability values at the nodes represent support values for BI and maximum likelihood (ML). For haplotype names, see Table 1.