Calcinus fuscus, Celia & Malay & Komai & Chan, 2012

Celia, Maria, Malay, D., Komai, Tomoyuki & Chan, Tin-Yam, 2012, A new cryptic species in the “ Calcinus anani Poupin & McLaughlin, 1998 ” species complex (Decapoda: Anomura: Diogenidae): evidence from colouration and molecular genetics *, Zootaxa 3367, pp. 165-175 : 167-172

Calcinus fuscus n. sp.

( Figs. 1, 2)

Calcinus purcher . — Miyake & Imafuku 1980: 5. [misspelling, not Calcinus pulcher Forest, 1958 ] Calcinus pulcher . — Miyake 1982, 1991, 1998: 114, pl. 38-5. — Asakura 1992: 39. [not Calcinus pulcher Forest, 1958 ] Calcinus anani . — Asakura & Tachikawa 2000: 267. — Kato & Okuno 2001: 69, unnumbered photograph. — Asakura 2002:

29, figs. 2–3, 21A. — Kawamoto & Okuno 2003: 74, 1 unnumbered photograph. — Poupin & Lemaitre 2003: 8 (in part).

— Okuno & Arima 2004: 54, fig. 2A. [not Calcinus anani Poupin & McLaughlin, 1998 ]

Material examined. Holotype: Kume Island , Ryukyu Islands, Japan, KUMEJIMA 2009, stn Trawl 71, 26°22.456ʹN, 126°42.232ʹE, 66–81 m, 19 November 2009, male SL 3.2 mm [RUMF-ZC-1520].

Paratypes: Ryugu , Ryukyu Islands , Japan, SCUBA, 30 m, 21 October 2001, 1 male SL 3.5 mm, [ CMNH-ZC 737 ]. Kume Island , Ryukyu Islands , KUMEJIMA 2009, stn Diving 6, near Aka-Todai , 26°21.225ʹN, 126°49.628ʹE, 15–30 m, 10 November 2009, 1 male SL 2.5 mm [ NTOU A00985]; stn Diving 18, Shogakko-mae , 26°20.012ʹN, 126°43.961ʹE, 18–39 m, 14 November 2009, 1 male SL 2.1 mm [ NTOU A00986]; stn Trawl 6, 26°23.044ʹN, 126°47.724ʹE, 64–81.3 m, 10 November 2009, 1 female SL 2.0 mm [ NTOU A01023 ]; stn Trawl 32, 26°16.775ʹN, 126°48.050ʹE, 67.3–73.3 m, 13 November 2009, 1 male SL 3.2 mm [ NTOU A01073 ]. Shionomisaki , Kii Peninsula , 30–40 m, lobster net, 11 March 1994, 1 female SL 3.4 mm [ CBM-ZC 4911 ]. Nazumado , Hachijo Island , Izu Islands , SCUBA, 40 m, 30 November 2000, 1 male SL 3.7 mm [ CMNH-ZC 516 ]; 45 m, 4 December 2000, 1 male SL 5.1 mm [ CMNH-ZC 517 ]; Akino-hama, Izu-oshima Island, 5 m, 12 February 2004, 1 male SL 5.7 mm [ CMNH-ZC 1704 ] .

Other material: Southeast Nang Island, Bismarck Archipelago, Papua New Guinea, SCUBA, 3–34 m, 3 July 2003, 1 male SL 4.2 mm [ UF 4808 ]; “joeles Reef” dive site, Kimbe Bay, SCUBA, 27 m, 17.vi.2003, 1 ovig. female SL 3.5 mm [ UF 11740 ]. Panglao Island , Bohol Province, Philippines, PANGLAO 2004, stn R47, Sungcolan , 9°38.8ʹN, 123°49.2ʹE, 4–25 m, 16 June 2004, 1 female SL 3.0 mm [ ZRC]; stn R63, Napaling , 9°37.2ʹN, 123°46.4ʹE, 3–40 m, 24 June 2004, 1 male SL 3.2 mm [ ZRC]; stn B9, Napaling , 9°33.1ʹN, 123°44.0ʹE, 8.5–10 m, 8 June 2004, 1 ovig. female 5.6 mm [ ZRC]; stn B15, Sungcolan , 9°38.8ʹN, 123°49.2ʹE, 2–4 m, 16 June 2004, 2 males SL 3.0– 4.6 mm [ ZRC]; stn B32, Looc , 9°35.8ʹN, 123°44.6ʹE, 20 m, 26 June 2004, 2 males SL 4.0– 4.1 mm [ ZRC]; stn B36, north of Doljo , 9°35.9ʹN, 123°44.5ʹE, 24 m, 1 July 2004, 1 female SL 2.5 mm [ ZRC]; stn B39, Pontod Lagoon 1 outside, 9°32.8ʹN, 123°42.1ʹE, 17–25 m, 3 July 2004, 2 females SL 3.4–4.6 mm [ ZRC]; stn B42, between Momo and Napaling, 9°37.0ʹN, 123°46.0ʹE, 30–33 m, 6 July 2004, 1 male SL 4.1 mm [ ZRC]. Lifou , Loyalty Islands, New Caledonia, LIFOU 2000, stn 1463, Santal Bay , 20°55.05ʹS, 167°03.35ʹE, 20–30 m, 10 November 2000, 1 female SL 2.0 mm [MNHN-IU-2011-70] .

Comparative material examined. Calcinus anani: Moruroa Atoll, Tuamotus, RV Marara , stn D51, 21°53.1ʹS, 139°02.6ʹW, 140 m, 15 October 1990, 1 male SL 5.9 mm, holotype [MNHN-IU-2008-15483]. Nuku Hiva Island, Marquesas, RV Marara , stn D79, 8°57.6ʹS, 140°05.8ʹW, 59 m, 22 January 1991, 1 male SL 2.1 mm [MNHN-IU- 2008-15592]; MUSORSTOM 9, stn DW1170, 08°45.1ʹS, 140°13.1ʹW, 104–109 m, 25 August 1997, 6 males SL 1.6–3.6 mm, 1 ovig. female SL 2.1 mm, 1 female SL 1.8 mm, paratypes [ MNHN Pg5561]; MUSORSTOM 9, stn DW1170, 08°45.1ʹS, 140°13.1ʹW, 104–109 m, 25 August 1997, 1 male SL 3.5 mm [MNHN-IU-2008-15485]; MUSORSTOM 9, stn DW1170, 08°45.1ʹS, 140°13.1ʹW, 104–109 m, 25 August 1997, 1 male SL 3.1 mm [MNHN- IU-2011-5104]; stn DR1181, 08°45.5ʹS, 140°03.2ʹW, 102–130 m, 26 August 1997, 1 ovig. female SL 2.0 mm [MNHN-IU-2008-16591]; stn CP1228, 09°44.6ʹS, 138°51.5ʹW, 107–108 m, 30.viii.1997, 1 male SL 2.8 mm [MNHN-IU-2008-16594]. Ua Pou Island , MUSORSTOM 9, stn CP1265, 9°20.4ʹS, 140°07.3ʹW, 3 September 1997, 90– 92 m, 1 ovig. female SL 1.7 mm, 1 male SL 1.7 mm [MNHN-IU-2008-16589]; stn. DW1143, 09°20.9ʹS, 140°02.7ʹW, 18–55 m, 22 August 1997, 1 ovig. female SL 1.8 mm [MNHN-IU-2008-16593]. Eiao Island , MUSORSTOM 9, stn DW1154, 07°58.50ʹS, 140°43.70ʹW, 102 m, 23 August 1997, 1 male SL 3.7 mm [ UF 15210 ( MNHN Pg6357 exchange)] .

Etymology. The Latin name fuscus (dark, dusky) refers to the brown colouration of the chelipeds.

Description. Shield about 1.1 times longer than wide; anterior margin between rostrum and lateral projections slightly concave. Rostrum broadly triangular with subacute tip, reaching or slightly overreaching small lateral projections.

Ocular peduncles 0.8–1.0 length of shield, slightly wider at base, subequal. Ocular acicles subtriangular, usually with a single terminal spine, rarely bifid.

Antennular peduncles not reaching distal corneal margins.

Antennal peduncles reaching distal 0.2–0.3 of ocular peduncles. Basal segment with ventrolateral distal angle bearing 1–5 small spines or finely crenulate. Second segment with short dorsomesial distal spine, dorsolateral distal angle produced, reaching midlength of acicle, terminating in simple or bifid spine. Third segment with 1 spine on ventromesial distal angle. Fourth segment with 1 small spine on dorsodistal margin. Fifth segment unarmed. Antennal acicle terminating in strong spine, dorsomesial margin with 3–4 strong spines distally, dorsolateral margin with 1 or 2 spines distally.

Left cheliped larger than right. Left chela (including fixed finger) 1.3–1.6 times longer than wide. Dactyl 0.4–0.6 times length of palm, with 2 rows of tubercles on upper face, cutting edge with 2 or 3 triangular calcareous teeth. Fixed finger with 2 or 3 triangular calcareous teeth on cutting edge. Palm with outer face regularly convex, finely granular, with single to several small spines at dorsodistal corner; upper margin with 6–8 (rarely 10) spines, spines sometimes eroded, or sometimes even with 2 or 3 additional smaller spines interspersed; lower face with large rounded or squamous tubercles, particularly at distal part and on fixed finger, tubercles rarely forming ridge; inner surface smooth, flattened, with a few small spines occasionally bearing setae adjacent to upper margin. Carpus with strong spine at about middle portion of outer surface, several low tubercles also scattered on outer and inner surfaces; upper margin with 3–6 spines forming ridge; distal margin bearing row of large tubercles. Merus with rows of small spines on ventrolateral and ventromesial margins, dorsodistal margin occasionally with 2 small denticles on outer side; lateral and mesial surfaces scattered with small tubercles.

Right chela (including fixed finger) 1.3–1.8 times longer than wide. Dactyl 0.6–0.9 times length of palm, with 2 irregular rows of tubercles on upper face, cutting edge with 2 or 3 triangular calcareous teeth. Fixed finger with 2 or 3 calcareous teeth on cutting edge. Palm with outer face weakly convex, finely granular, with 4 or 5 spines near base of dactyl; upper margin with 5 or 6 strong spines; lower face with few low tubercles; inner surface smooth, flattened, with small spines adjacent to upper margin. Carpus with 2–4 spines on upper margin, these spines increasing in size distally; inner and outer surfaces with scattered small tubercles; distal margin with row of low tubercles. Merus unarmed on ventrolateral and ventromesial margins, or with 2–4 small spines subdistally; dorsodistal margin unarmed or armed with 2 or 3 small spines on lateral side.

Ambulatory legs similar on left and right sides. Second pereopod exceeding left cheliped by length of dactyl and distal tenth of propodus. Dactyl of left pereopod 0.6–0.9 times as long as propodus; ventral margin with widely-spaced tufts of long setae and 8–13 corneus spines. Propodus with scattered tufts of setae, usually with 1 or 2 small subdistal corneus spines on ventral margin. Carpus 0.6–0.9 times length of propodus, with 1–3 spines on dorsodistal angle. Merus usually with small denticles on distal third of ventral margin (more common on right pereopods) and 0–1 (mostly 1) small spine on ventrodistal lateral angle.

Dactyl of left third pereopod 0.7–0.8 times as long as propodus; ventral margin bearing 6–7 corneus spines, and tufts of long setae that usually form dense brush, but occasionally rather sparse. Propodus with 2 or 3 small corneus spines on ventral margin subdistally, ventral face with widely spaced tufts of long setae on distal half. Carpus 0.6–0.7 times length of propodus, with 1 or 2 spines on dorsodistal angle. Merus sometimes with small spine on ventrodistal lateral angle.

Telson with posterior lobes slightly to strongly asymmetrical, left lobe 1.1–1.6 times longer than right lobe. Terminal margins each with fringe of long setae, left lobe with 1 inwardly curved spine, right lobe usually with 1 spine (sometimes unarmed).

Colouration. Shield reddish-brown, occasionally white with reddish-brown markings, outer border light orange. Proximal two segments of antennular peduncles brown, third segment and flagellum yellow. Ocular peduncles orange proximally, progressively fading to yellowish-white distally; corneas black; ocular acicles orange. Antennal acicles white, second to fourth segments of antennal peduncle brown, fifth segment yellow, flagella transparent. Palms of chelipeds purplish-gray to gray, progressively fading to white in fingers; meri and carpi dark reddish-brown with scattered white spots; distal margin of carpi with a ring of white spots. Second to fifth pereopods generally orange, covered with white to light purple reticulated stripes and spots; reticulated pattern on second and third pereopods comprised of long stripes proximally and short stripes or spots distally. Telson mostly white.

Distribution. Western Pacific, known with certainty from Japan (Izu Islands, Kii Peninsula, and Ryukyu Islands), the Philippines (Panglao Island in the Central Visayas), Papua New Guinea ( Bismarck Archipelago) and New Caledonia (Lifou), at depths of 2–81 meters.

Remarks. Calcinus fuscus n. sp. and C. anani belong to the Clade X of Calcinus in Malay & Paulay (2010: fig. 1A), which is comprised mainly of deep-water and high-latitude species. Based on limited collections in Japan, previous authors suggested some possible morphological differences between the Japanese and the typical forms of C. anani ; namely the degree of setation of the third pereopods ( Asakura 2002), length of the rostrum ( Okuno & Arima 2004), and the structure of the telson ( Okuno & Arima 2004). However, the present examination of more specimens from Japan and other western Pacific localities, as well as re-examination of the topotypic material from French Polynesia, revealed that these characters are actually quite variable. For example, the left lobe of the telson was reported as strongly protruded in the Japanese specimens ( Asakura 2002: fig. 3J) and as nearly equal in size in the type material ( Poupin & McLaughlin 1998: fig. 1e). However the present series of specimens showed that the left posterior lobe of the telson is 1.1–1.6 times longer than the right lobe in both the western Pacific and French Polynesian materials. The only noticeable character differing between the western Pacific and French Polynesian populations is the colouration of the chelipeds. In C. fuscus n. sp. ( Fig. 2), the meri and carpi of the chelae are dark brown and scattered with some white spots, the palms are purplish gray or gray and fading distally to white fingers. There is a sharp break in colouration at the distal margins of the carpi, and this border is also marked by a ring of distinct whitish tubercles. In contrast, in C. anani the chelae are more or less orange overall, progressively fading to a slightly paler colour distally. Calcinus anani was in fact named after its generally orangeish body colour ( Poupin & McLaughlin 1998).

The genus Calcinus is known to evolve interspecific colour differences remarkably rapidly ( Malay & Paulay 2010). Even in the absence of diagnostic morphological characters, colouration is a reliable indicator of species boundaries in Calcinus [e.g., C. elegans (H. Milne Edwards, 1836) versus C. orchidae Poupin, 1997 (cf. Poupin 1997); C. gouti Poupin, 1997 versus C. hakahau Poupin & McLaughlin, 1998 (cf. Poupin & McLaughlin 1998); C. gaimardii (H. Milne Edwards, 1848) versus C. morgani Rahayu & Forest, 1999 (cf. Rahayu & Forest 1999); C. californiensis Bouvier, 1898 versus C. mclaughlinae Poupin & Bouchard, 2006 (cf. Poupin & Bouchard 2006)]. Moreover, cryptic species that barely differ morphologically yet are distinct in colour patterns are rather common throughout decapod crustaceans such as in the other hermit crab genera Clibanarius bimaculatus De Haan, 1849 versus C. rubroviria Rahayu, 1999 and C. arethusa De Man, 1888 versus C. rutilus Rahayu, 1999 ( Rahayu 1999) ; Ciliopagurus strigatus ( Herbst, 1804) complex ( Poupin & Malay, 2009); porcelain crabs Petrolisthes galathinus ( Bosc, 1802) complex ( Hiller et al. 2006); squat lobsters Raymunida spp. Macpherson and Machordom, 2000 ( Macpherson & Machordom 2001); peppermint shrimp Lysmata wurdemanni ( Gibbes, 1850) complex ( Rhyne & Lin 2006); alpheid shrimp Alpheus tricolour Anker, 2001 versus A. fasqueli Anker, 2001 ( Anker 2001) .

Figure 3 plots the mean pairwise K2P distance for sister species in the genus Calcinus (data based on Malay & Paulay 2010). Although there is no “barcoding gap” demarcating intraspecific vs. interspecific genetic distances in this genus, this agrees with previous observations in some other marine invertebrate groups ( Meyer & Paulay 2005). The average K2P genetic distance separating the Western Pacific C. fuscus n. sp. from the South Pacific C. anani specimens is 6.31% (±0.37%). This clearly falls within the range of interspecific genetic distances for Calcinus ( Fig. 3, see also Malay & Paulay 2010). On the other hand, average genetic distance within clades is only 1.38% (±0.39%), falling within the range for intraspecific distances for Calcinus as shown in Fig. 3. Thus, the Western Pacific populations should have a distinct specific status and warrant a new name.

The COI phylogram for C. fuscus n. sp. and C. anani is presented in Fig. 4. Calcinus fuscus n. sp. is again distinct from C. anani , with the latter species forming a monophyletic clade. On the other hand, C. fuscus n. sp. is not reciprocally monophyletic with C. anani , but rather forms a paraphyletic grade from which C. anani arises. This topology (i.e., a polytomy with a strongly supported Polynesian clade arising from within the polytomy) is concordant with a scenario where the Western Pacific C. fuscus n. sp. gave rise to the Polynesian C. anani through peripheral speciation. In fact, peripatric speciation at the range peripheries of older and more widespread taxa is the dominant mode of speciation in Calcinus ( Malay & Paulay 2010) . Recently separated sister species pairs are expected to show a lower degree of differentiation in biological traits (morphological, genetic, reproductive, etc.) than older sister species pairs. As two lineages diverge, they pass through polyphyletic and paraphyletic stages before finally reaching reciprocal monophyly ( de Queiroz 1998; 2007). Monophyly can only be applied to terminal taxa but not ancestral lineages, because ancestors by definition are non-monophyletic ( de Queiroz 1998). In the present case, the non-monophyly of the ancestor C. fuscus n. sp. can be deemed a logical consequence of the recent peripatric speciation of C. anani . Such a paraphyletic ancestor having wide geographical distribution with recently separated monophyletic peripheral sister species is also applied to the polar bear Ursus maritimus Phipps, 1774 and the widely distributed brown bear U. arctos Linnaeus, 1758 (see Rieppel 2009).

Other than the colouration and genetics, Calcinus fuscus n. sp. appears to differ from C. anani in vertical and geographical distributions. Available information shows that Calcinus anani occurs in deeper waters and is mainly collected from trawls and dredges at depths of more than 100 m (deepest records are at depths of 230–262 m and shallowest at 18–55 m). In contrast, Calcinus fuscus n. sp. is mainly collected by diving. Some specimens were also collected by shallow water trawling from less than 82 m. Most Calcinus species have well defined ecological niches with narrow depth ranges ( Malay & Paulay 2010).

Calcinus fuscus n. sp. is known from Japan, the Philippines, Papua New Guinea, and New Caledonia, while the true C. anani seems to be restricted to Polynesia (Tuamotus, Marquesas, and the Austral Islands). Asakura & Nomura (2001) considered that a record of C. pulcher Forest, 1958 , from Palau ( Baba 1982) should be referred to as “ C. anani ”. However, Baba (1982) described the colouration of the Palau material as “Spots on walking legs, orange in alcohol, remain as figured by Forest (1958: fig. 16).” This is the typical spots and stripes colouration of C. pulcher , and cannot be mistaken for the colour patterns of either C. anani or C. fuscus n. sp. Thus, it is highly likely that Baba’s (1982) record of C. pulcher from Palau was correct.

Asakura (2002) suggested that C. anani and C. sirius Morgan, 1991 (the latter known only from Norfolk and Lord Howe Islands) might be conspecific, because he did not find significant morphological differences between the Japanese specimen he referred to as “ C. anani ” and the three paratypes of C. sirius . Nevertheless, as Poupin & McLaughlin (1998) noted, the different colour pattern of the ambulatory legs seems to provide evidence to distinguish C. anani and the present new species from C. sirius . Furthermore, comparison between the present material of C. fuscus n. sp. and C. anani with the original description of C. sirius shows that the upper margin of the right palm is more strongly spinose in C. sirius than in the new species and C. anani . While the colouration in life is not known for C. sirius, Morgan (1991) nonetheless noted that the shield of C. sirius has darker anterior and lateral margins; in contrast the shield margins are distinctly paler than the shield center in C. fuscus n. sp. The ocular peduncles in C. sirius were mentioned as deep brown in the proximal half, whereas they are paler-coloured in C. fuscus n. sp. and C. anani . In C. sirius , there is marked sexual dimorphism in the left chela, which has more developed spines and tubercles but less distinct gap between the dactyl and fixed finger in females. Such sexual dimorphism is not found in C. anani and C. fuscus n. sp. Finally, the body size of C. sirius appears to be larger than C. anani and C. fuscus n. sp. Of the 16 specimens known for C. sirius , the largest is SL 6.9 mm ( Morgan 1991). The largest specimens of C. anani and C. fuscus n. sp. are SL 5.9 mm and 5.7 mm, respectively.