Research Article |
Corresponding author: Chien-Hui Yang ( chyang@ntou.edu.tw ) Academic editor: Ingo S. Wehrtmann
© 2021 Peter K. L. Ng, Chien-Hui Yang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ng PKL, Yang C-H (2021) On two new species of deep-sea carrier crabs (Crustacea, Brachyura, Homolodromiidae, Dicranodromia) from Taiwan and the Philippines, with notes on other Indo-West Pacific species. ZooKeys 1072: 129-165. https://doi.org/10.3897/zookeys.1072.72978
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The systematics of four species of the homolodromiid genus Dicranodromia A. Milne-Edwards, 1880, from East Asia and the Philippines is reappraised: D. danielae Ng & McLay, 2005, D. doederleini Ortmann, 1892, D. karubar Guinot, 1993, and D. martini Guinot, 1995; and key characters such as the epistome, gonopods, and spermatheca are figured in detail. Two new species, D. erinaceus sp. nov. and D. robusta sp. nov., are described from Taiwan and the Philippines, respectively. Dicranodromia erinaceus sp. nov. resembles D. spinulata Guinot, 1995, and D. delli Ahyong, 2008 (from New Caledonia and New Zealand) but can be separated by its distinctly spinulated carapace surfaces and proportionately shorter fifth ambulatory legs. Dicranodromia robusta sp. nov. is superficially similar to D. baffini (Alcock & Anderson, 1899) and D. karubar Guinot, 1993, but can easily be separated by possessing a broad dorsoventrally flattened infraorbital tooth. A genetic study of the species using the mitochondrial cytochrome c oxidase I gene confirms that the taxa are distinct, with D. erinaceus sp. nov. coming out in a well-supported clade from congeners. The megalopa of D. doederleini is also reported for the first time.
Comparative taxonomy, deep-sea crab, East Asia, Homolodromioidea, systematics.
The deep-water carrier crabs of the homolodromiid genus Dicranodromia A. Milne-Edwards, 1880, are represented by 20 species from the Atlantic, Indian, and Pacific Oceans (
We describe two additional species from Taiwan and the Philippines. The Taiwanese material had been misidentified as “D. doederleini” by earlier workers, while the Philippine specimens had been incorrectly identified by field collectors as “D. delli”. We also take this opportunity to update the character states of some poorly known species and refigure them so that they are better defined. In particular, we add male first and second gonopod characters for the species as they are useful to discriminate some of the taxa. Their taxonomy is also discussed. In addition, we also report on the larvae of an ovigerous female of D. doederleini which had been kept in the aquarium.
Material examined is deposited in the National Taiwan Ocean University (
The terminology used follows
For the molecular analysis, a total of seven individuals were used (as indicated on the material examined of each species below). Two species, D. danielae and D. robusta sp. nov., could not be tested as they had originally been preserved in formalin. Crude genomic DNA was extracted from the muscles of the pleon using QIAamp DNA Micro Kit (Qiagen, Cat. No. 56304, Valencia, CA, USA) following the protocol of the manufacturer. The DNA barcoding gene (mitochondrial cytochrome c oxidase I, COI; cf.
The resulting sequences were firstly translated into the corresponding amino acids by EditSeq (LASERGENE; DNASTAR) to check for pseudogenes (
Dicranodromia ovata A. Milne-Edwards, 1880, by monotypy; gender feminine).
As the number of species has increased and more material has been examined since the revision by
1 | Basal antennal article relatively short, stout; anteroexternal tooth long, subequal to or longer than rest of article | 2 |
– | Basal antennal article more elongate; anteroexternal tooth short, distinctly shorter than rest of article | 7 |
2 | Carapace and pereiopods covered with short and very dense plumose setae, forming velvet-like tomentum, obscuring surfaces and margins of pereiopods | 3 |
– | Setae of various types and lengths on carapace and pereiopods, can be relatively dense but never obscuring surfaces and margins of pereiopods | 4 |
3 | Carapace proportionately wider, anterolateral and posterolateral margins unarmed or only with small granules [southern Java and Moluccas] | D. karubar Guinot, 1993 |
– | Carapace proportionately narrower, anterolateral and posterolateral margins lined with sharp spinules or granules [Indian Ocean] | D. baffini (Alcock & Anderson, 1899) |
4 | Infraorbital tooth broad, dentiform to linguiform, subequal or larger than exorbital tooth [Philippines] | D. robusta sp. nov. |
– | Infraorbital tooth triangular, smaller than exorbital tooth | 5 |
5 | Anterior surface of epistome prominently spinose; P2 and P3 merus with distinct spines on flexor margin [Philippines] | D. danielae Ng & McLay, 2005 |
– | Anterior surface of epistome at most granulate or with scattered spinules; flexor margin of P2 and P3 merus unarmed | 6 |
6 | P2 and P3 dactyli short, propodus more than twice length of dactylus [Philippines] | D. chenae Ng & Naruse, 2007 |
– | P2 and P3 dactyli long, propodus 1.5–1.6× length of dactylus carapace [Philippines] | D. martini Guinot, 1995 |
7 | Dorsal surface of carapace covered with distinct spinules, especially along lateral parts, those on median parts may be present as granules; flexor margin of P2–P5 merus distinctly lined with spines | 8 |
– | Dorsal surface of the carapace almost smooth, with granules or spinules present only on lateral parts; P2 and P3 merus unarmed except for flexor margin sometimes with spinules, P4 and P5 merus unarmed | 11 |
8 | Exorbital tooth exorbital tooth triangular, dentiform; posterior margin of epistome prominently spinose [Madagascar] | D. crosnieri Guinot, 1995 |
– | Exorbital tooth slender, spiniform; posterior margin of epistome entire, adjacent area smooth or with scattered spinules | 9 |
9 | Median part of dorsal surface of carapace covered with distinct spinules; submarginal area of posterior margin of epistome with several spinules; P2 and P3 relatively short (e.g., P3 propodus less than 7× longer than wide; propodus 1.7× length of dactylus) [New Caledonia; New Zealand] | D. spinulata Guinot, 1995 |
– | Median part of dorsal surface of carapace covered with granules, not spinules; submarginal area of posterior margin of epistome unarmed; P2 and P3 relatively longer (e.g., P3 propodus more than 8× longer than wide; propodus 1.7× length of dactylus) | 10 |
10 | P2–P5 proportionately shorter (e.g., P3 merus 4.5× longer than wide; P5 merus just reaching branchiocardiac groove when folded dorsally) [Taiwan] | D. erinaceus sp. nov. |
– | P2–P5 proportionately longer (e.g., P3 merus 6.6× longer than wide; P5 merus longer and more slender, extending beyond branchiocardiac groove when folded dorsally) [New Zealand] | D. delli Ahyong, 2008 |
11 | Posterior margin of epistome entire; outer surface of palm in both sexes evenly covered with granules [Chesterfield Islands] | D. foersteri Guinot, 1993 |
– | Posterior margin of epistome crenulate; median outer surface of palm in both sexes smooth, granules only present on subdorsal and subventral margins | 12 |
12 | Carapace and pereiopods covered with numerous long stiff setae but not obscuring surfaces and margins [known for certain only from Japan] | D. doederleini Ortmann, 1892 |
– | Carapace and pereiopods densely covered with numerous setae of different types; partially obscuring carapace surface and margins, but almost completely obscuring surfaces and margins of pereiopods [Japan] | D. nagaii Guinot, 1995 |
Dicranodromia doederleini
Ortmann, 1892: 549, pl. 26, fig. 4;
Japan: 1 ♀ with 1 megalops (15.9 × 20.2 mm), Sagami Bay, from aquarium trade, 8 Apr. 2015 (
This species is well known (for synonymy and records, see
One female specimen (
Dicranodromia doederleini Ortmann, 1892, ♀ (15.9 × 20.2 mm) (
Dicranodromia doederleini Ortmann, 1892, ovigerous ♀ (14.5 × 19.2 mm) (
The observations above on the eggs and megalopa of D. doederleini provide some clarity on the larval development in the genus. While it is known the eggs are large and the development is abbreviated, it is not sure of the eggs hatch into an advanced zoeal stage or directly into megalopa.
Dicranodromia martini
Guinot, 1995: 221, figs 19a–e, 20A–C;
Philippines: l ♂ (12.3 × 16.6 mm), station CP2396, 9°36.3'N, 123°42.0'E, Maribohoc Bay, Panglao, Bohol, Visayas, 609–673 m, PANGLAO 2005 Expedition, coll. MV DA-BFAR, 31 May 2005 (
Colour in life. A,B Dicranodromia karubar Guinot, 1993, ♂ (28.7 × 34.7 mm) (
Dicranodromia karubar
Guinot, 1993: 213, figs 15A–C, 16A–D, 25A, B;
Indonesia: 1 ♂ (28.7 × 34.7 mm), 3 ovigerous ♀♀ (24.8 × 31.5 mm, 27.1 × 33.4 mm, 27.6 × 33.8 mm), station CP39, 8°15.885'S, 109°10.163'E – 8°16.060'S, 109°10.944'E, 528–637 m, substrate partially muddy, plenty of glass sponges, echinoderms, polychaeta, galatheids, fishes, sea anemone, gastropods and bivalves, south of Cilacap, south Java, Indian Ocean, South Java Deep Sea cruise, coll. beam trawl, 30 Mar. 2020 (
Dicranodromia karubar Guinot, 1993. A–H, J ♀ (27.1 × 33.4 mm) (
The setae on D. karubar are unusual in that they are plumose at the distal part (
Dicranodromia karubar can easily be separated from D. baffini by its proportionately broader carapace (Figs
Dicranodromia karubar is known thus far only from the Moluccas and eastern part of the Indian Ocean while D. baffini has been recorded from western India, Maldives and Andamans (
All the females of D. karubar collected from the south Javan cruise were ovigerous, the eggs being bright red in life, in a prominent brood pouch (Fig.
Dicranodromia danielae
Ng & McLay, 2005: 40, figs 1–4;
Philippines: holotype ovigerous ♀ (broken, 10.8 × 14.2 mm), Balicasag Island, Panglao, Bohol, Visayas, in tangle nets, ca. 200–300 m, coll. local shell fishermen, 2 Mar. 2004 (
The broken holotype female was re-examined and some characters need to be added or amended from
Dicranodromia danielae Ng & McLay, 2005, holotype ovigerous ♀ (broken, 10.8 × 14.2 mm) (
Some of the characters of D. danielae resemble the male specimen 9.7 × 14.0 mm from Uraga Strait in Japan (35°4.833'N, 139°38.3'E) which
Dicranodromia doederleini
–
TAIWAN: holotype ♀ (14.0 × 18.0 mm), station CP4091, 22°14'N, 119°59'E, among numerous mud tubes, off small Liu-Qiu Island, southeast Taiwan, 974–994 m, coll. N.O. Ocean Researcher 1, 27 May 2013 (
Carapace longitudinally subovate, widest across intestinal-mesobranchial regions; dorsal surface prominently convex, lateral surfaces covered with numerous spinules, those on median part relatively lower, sometimes granular, with short stiff setae, denser on lateral parts but not obscuring margins; short stiff setae present on pereiopods, thoracic sternum and pleon but not obscuring surface or margins. Branchiocardiac groove distinct, curving medially anteriorly. Each pseudorostral lobe triangular, inner margin straight, outer margin gently convex, directed anteriorly, inner margin with two or three spinules; exorbital tooth spiniform, directed obliquely laterally, anterior margin with two or three spinules; supraorbital margin separated from external orbital tooth by shallow concave cleft, posterior part with three spines; infraorbital margin with prominent triangular lobe, posterior margin with spinules, just visible in dorsal view. Rostrum present as one or two longer spinules in small specimens, barely discernible or just visible as a sharp granule in larger specimens. Epistome covered with spinules on anterior half; posterior half gently upturned, with median fissure, surface not covered with spinules, posterior margin entire. Basal antennal article subquadrate; surfaces covered by spinules and granules; anteroexternal tooth short. Eyes with short peduncle. Third maxilliped relatively narrow; merus subovate with low anterointernal lobe, slightly shorter than ischium; ischium subtrapezoidal, distal half wider than proximal part with inner margin convex; palp (carpus, propodus, dactylus) long, reaching to median part of ischium when folded; exopod with proximal third widest, outer margin with low sharp granules on proximal third. Chelipeds densely covered with stiff setae on most parts; merus and carpus with outer surface and margins lined with spinules and granules; palm relatively short, outer surface and margins covered with numerous sharp granules; fingers thick, wide, occluding surface hollowed; pollex with deep U-shaped depression distally. P2 and P3 relatively long, P3 longer than P2; merus with low tooth on distal extensor margin, length to width ratio of P2 and P3 merus 5.2 and 4.5, respectively; proximal part of extensor margin with low spinules, flexor margin with numerous spinules; propodus almost straight, unarmed, length to width ratio of P2 and P3 propodus 6.7 and 8.0, respectively; dactylus sickle-shaped, flexor margin lined with 15 or 16 spines, terminating in strongly incurved claw, propodus about twice length of dactylus. P4 stouter, shorter than P5; length to width ratio of P4 and P5 merus 3.5 and 5.0, respectively; proximal part of extensor margin of merus with low spinules, flexor margin with numerous spinules; P4 and P5 propodus without median spinules on outer surface, length to width ratio of P4 and P5 propodus 3.5 and 4.7, respectively, distal margin fringed by sharp spines bracketing dactylus; dactylus claw-like, strongly incurved, extensor margin unarmed, flexor margin unarmed or with two weak spines. Thoracic sternite 7 with strong transverse ridge from posterior inner part of female gonopore, lateral part raised, forming triangular tubercle, curving posteriorly to join oblique ridge formed by sternites 7 and 8 with distinct groove between them that leads to spermathecal aperture at centre of triangular tubercle. Male and female pleons with six free somites and telson; male telson distinctly subovate; female telson wide, triangular, with gently sinuous margins. G1 stout, endopod distally covered by dense long setae, subdistal part of outer margin with two lobes, proximal lobe larger, prominent; G2 endopod gradually tapering to sharp tip.
Dicranodromia erinaceus sp. nov. A–E holotype ♀ (14.0 × 18.0 mm) (
None of the specimens examined had a spine or spinule on the extensor margin of the P5 dactylus; and outer surface of the P5 propodus was also unarmed (Fig.
The species is named after the hedgehog, Erinaceus, alluding to the spiny appearance of the carapace and legs. The name is used as a noun in apposition.
Dicranodromia erinaceus sp. nov. belongs to the same group of species as D. spinulosa and D. delli in its spinose carapace surface and pereiopods, slender and spiniform exorbital tooth, and an acutely triangular suborbital tooth. Dicranodromia erinaceus is most similar to D. delli from New Zealand but can be distinguished by the ischium of the third maxilliped being relatively shorter and wider especially at the distal half (Fig.
Compared to D. spinulosa, D. erinaceus can be separated by the carapace being proportionately wider (Figs
Philippines: Holotype ♀ (19.6 × 26.4 mm), ca. 5°24'N, 125°22.5'E, Balut Island, Sarangani Islands, Davao Occidental Province, south of Mindanao Island, coll. tangle nets, local fishermen, 26 Nov. 2017 (
Carapace longitudinally subquadrate, widest across intestinal-mesobranchial regions; dorsal surface gently convex, lateral surfaces covered with low spinules, median part smooth, margins with scattered short stiff setae, not obscuring margins; short stiff setae present on pereiopods, thoracic sternum and pleon but not obscuring surface or margins. Branchiocardiac groove distinct, curving medially anteriorly. Each pseudorostral lobe triangular, inner margin straight, outer margin gently convex, directed anteriorly, inner margin entire; exorbital tooth dentiform, directed obliquely laterally, anterior margin with two or three spinules; supraorbital margin separated from external orbital tooth by shallow concave cleft, posterior part with five or six spinules; infraorbital margin with large dorsoventrally flattened lobe which is dentiform to linguiform, larger than exorbital tooth, distal part with spine, anterior margin with two spinules, prominently visible in dorsal view. Rostrum present as one sharp granule. Epistome covered with scattered granules on anterior half; posterior half gently upturned, with median fissure, surface not covered with spinules, posterior margin gently convex, median part entire, lateral part gently serrate. Basal antennal article subquadrate; surfaces covered by spinules and granules; anteroexternal tooth short. Eyes with long peduncle. Third maxilliped relatively narrow; merus subovate with low anterointernal lobe, shorter than ischium; ischium subtrapezoidal, distal half slightly wider than proximal part; palp (carpus, propodus, dactylus) long, reaching to median part of ischium when folded; exopod with proximal third widest. Chelipeds covered with stiff setae on most parts; merus and carpus with margins uneven or lined with granules; palm relatively short, subdorsal and subventral margins with low sharp granules, median part smooth; fingers thick, wide, occluding surface hollowed; pollex with deep U-shaped depression distally. P2 and P3 relatively short, P3 longer than P2; merus with low tooth on distal extensor margin, length to width ratio of P2 and P3 merus 4.2 and 3.9, respectively; margins unarmed; propodus almost straight, unarmed, length to width ratio of P2 and P3 propodus 5.2 and 6.4, respectively; dactylus curved, flexor margin lined with 8 or 9 spines, terminating in strongly gently curved claw, propodus about 2.4× length of dactylus. P4 stouter, shorter than P5; length to width ratio of P4 and P5 merus 2.4 and 3.4, respectively; margins of merus unarmed; P4 and P5 propodus with submedian spinule on distal third of outer surface, length to width ratio of P4 and P5 propodus 2.3 and 3.6, respectively, distal margin fringed by sharp spines bracketing dactylus; dactylus claw-like, strongly incurved, extensor margin with median spine or absent, flexor margin with 2–4 spines. Thoracic sternite 7 with low transverse ridge from posterior inner part of female gonopore, lateral part high, forming triangular tubercle, curving posteriorly to join oblique ridge formed by posterior part of sternite 7, just before suture with sternite 8, groove between sternites 7 and 8 curve to join spermathecal aperture at base of triangular tubercle. Male and female pleons with 6 free somites and telson; male telson distinctly elongate, triangular with gently convex lateral margins; female telson triangular, with gently convex margins. G1 stout, endopod distally covered by dense long setae, subdistal part of outer margin with two lobes, the distal one being more prominent; G2 endopod gradually tapering to sharp tip.
In the holotype female, the left P5 dactylus has a prominent spine on the extensor margin (Fig.
The species is named after the Latin robusta for stout, alluding to the stocky appearance of the species.
The most diagnostic character of D. robusta sp. nov. is the large dorsoventrally flattened infraorbital tooth, which is dentiform to linguiform, clearly visible in dorsal view, and distinctly larger than the exorbital tooth (Figs
The carapace shape of D. robusta is distinctly more quadrate (Figs
Compared to D. baffini from the Indian Ocean, D. robusta has a more quadrate carapace (Figs
A Dicranodromia erinaceus sp. nov., holotype ♀ (14.0 × 18.0 mm) (
Dicranodromia robusta can be separated from D. danielae in having the exorbital tooth distinctly triangular to linguiform (Figs
The armature of the posterior margin of the epistome is a useful character but must be used carefully as well. In species like D. danielae, the margin is prominently spinose even when viewed frontally, with spines appearing more prominent when the margin is viewed subventrally (Fig.
In general, all species have spinules on some part of the carapace and these are often surrounded by stiff setae which partially obscure the spinules. Cleaning must be done with great care as the spinules (and even some of the spines) are brittle and break easily.
The structures of the G1 and G2 have not been used to separate species and
The molecular analyses using COI sequences closely supported the morphological observations. There was some intraspecific divergence in the three individuals of D. doederleini tested (GenBank accession nos. OK351331-OK351333), ranging from 0–1.2%, while that in two specimens of D. erinaceus sp. nov. (accession nos. OK351334-OK351335) was 0.2%. In Dicranodromia, the divergence at the species level was 9.6–14.0%, with D. erinaceus sp. nov. distinct from the tested species by 12.8–14.0%. The outgroup H. kai (accession no. OK351338) has a minimal divergence of 12.6–12.8% with D. erinaceus sp. nov., and a maximal value of 14.2% with D. karubar. The maximum likelihood tree also showed D. erinaceus sp. nov. to form an independent clade from other Dicranodromia species with an extremely high support (MLb = 100) (Fig.
Noteworthy is that the Philippines has four species: D. danielae, D. chenae, D. martini and D. robusta sp. nov. Two of the species (D. chenae and D. martini) were collected by trawls, the substrate being more level and less rocky. Like D. danielae, D. robusta sp. nov. was collected by tangle nets set in deep-water, which may explain why it has not been collected until now. Deep-water habitats with steep rocky substrates are difficult to sample, and the fauna is often different from those occurring in flatter substrates (see
We thank T. Komai for his kind help with specimens. Paul Ng kindly passed us the specimen and shared the photographs of live D. doederleini. Thanks are due to Evelyn Antig (Palaone Trading) in the Philippines for help with and information on the two specimens from Mindanao. The SJADES cruise which obtained D. karubar was a joint Indonesian-Singapore expedition to southern Java funded by the National University of Singapore and the Research Center for Oceanography, Indonesian Institute of Sciences (LIPI), and supported by their respective Ministries of Foreign Affairs under the RISING 50 program to promote bilateral co-operation. We thank Bertrand Richer de Forges for his invaluable help with the cruise and trawling efforts, as well as Tin-Yam Chan and his team for their invaluable help in the trawling work and other support. We are also most grateful to Danièle Guinot, Tohru Naruse, and Shane Ahyong for their many suggestions which have improved the manuscript.