First record of a cold-seep squat lobster Munidopsis lauensis Baba and de Saint Laurent, 1992 (Anomura: Galatheoidea) from Indian watersAbstract
The present study reports the first zoogeographical record of the squat lobster Munidopsis lauensis Baba and de Saint Laurent, 1992 from a cold-seep site in the Krishna-Godavari Basin (Bay of Bengal), Northern Indian Ocean. Molecular analysis of the partial mitochondrial gene coding for cytochrome C oxidase subunit I (COI mtDNA), and mitochondrial 16S ribosomal RNA (16S rRNA) validated its identity. The present observation extends its geographical distribution to the Northern Indian Ocean. Additionally, molecular barcodes (COI) were generated for Munidopsis scobina Alcock, 1894, Munidopsis wardeni Anderson, 1896, and Shinkaia crosnieri Baba and Williams, 1998 collected from the Indian Exclusive Economic Zone.
Keywords
Bay of Bengal; deep-sea; morphology; Munidopsidae; new record
INTRODUCTION
The cold-seep ecosystem, originally discovered by Paull et al. (1984) in the abyssal plains (> 3,000 m) of the Gulf of Mexico, was subsequently reported from more than 150 active cold-seep sites globally (German et al., 2011). The first-ever documentation of a cold-seep environment in the Indian waters was made in the Krishna-Godavari basin (K-G basin), western Bay of Bengal, India (Mazumdar et al., 2019), which revealed the occurrence of methane gas hydrates at 2-3 m under the sea floor with a thriving community of chemosymbiont-bearing annelids, echinoderms, crustaceans, and molluscs (Mazumdar et al., 2019; Sangodkar et al., 2022). Gonsalves et al. (2022) reported the first occurrence of the hydrothermal vent and cold-seep inhabiting monotypic squat lobster, Shinkaia crosnieriBaba and Williams, 1998, from this site.
The squat lobster genus MunidopsisWhiteaves, 1874 is represented by 32 species in Indian waters (Patel et al., 2022; Tiwari et al., 2022a ; 2022b). In this study, Munidopsis lauensis, a hydrothermal vent and cold-seep inhabitant of the western Pacific and the Central Indian oceans (Hwang et al., 2022), is recorded for the first time from a cold-seep site in the Indian Exclusive Economic Zone (Fig. 1) based on morphological and molecular analyses.
Map indicating the known geographical distribution of Munidopsis lauensisBaba and Saint Laurent, 1992. Symbols in red denote hydrothermal vent sites, those in blue denote cold-seep sites. (- type locality; ( - present study area; ( - hydrothermal vent location; ( - cold-seep location.
MATERIAL AND METHODS
The squat lobster specimens examined during this study were collected during the Research Vessel Sindhu Sadhana cruise number SSD-045 (March 2018) (Fig. 1), using a box corer from 1,754.5 m depth in the K-G Basin, Bay of Bengal, India. The specimens were then cleaned of debris, photographed, and preserved in 80% ethanol. Taxonomic identification followed the identification key provided by Baba (2005). Photographic and line illustrations were prepared using Adobe® Photoshop CS5. Morphometric measurements of the carapace and pereopods were carried out using vernier callipers with an accuracy of 0.1 mm.
Morphological terminology used in this study followed Baba et al. (2009). The specimen size was defined by (i) the length of the postorbital carapace, measured along the dorsal midline from the posterior margin of the orbit to the posterior margin of the carapace, and (ii) the maximum width of the carapace. The specimens were deposited, as reference voucher samples, in the National Repository for Marine Flora and Fauna at CSIR-National Institute of Oceanography (NIO), Dona Paula, Goa, India.
The isolation of the genomic DNA from the pereopod tissue was done using the DNeasy Blood and Tissue (Qiagen) kit following the manufacturer’s protocol. Universal primer LCO1490/HCO2198 was used to amplify the partial mitochondrial cytochrome oxidase subunit I (COI) by polymerase chain reaction (PCR) (Folmer et al., 1994). Similarly, Palumf-16s/ Palumr-16s was used to amplify the partial mitochondrial 16S rRNA (Palumbi, 1996). The editing and alignment of the obtained DNA sequences were done using the BioEdit sequence alignment editor version 5.0.9 (Hall, 1999). Except for M. lauensisBaba and de Saint Laurent, 1992, Munidopsis scobinaAlcock, 1894, and Munidopsis wardeni Anderson, 1896 sequenced in this study, other Munidopsis sequences (M. dasypus Alcock, 1894, M. trifida Henderson, 1885; see Tab. 1 for GenBank accession number) obtained from the GenBank database were used for comparative and phylogenetic analyses.
Accession number, and reference details of the species used in phylogenetic tree for COI genes.
The evolutionary history was inferred by using the Maximum Likelihood method and Tamura 3-parameter model. The tree with the highest log likelihood (-2111.58) is shown. Initial tree(s) for the heuristic search were obtained automatically by applying the Maximum Parsimony method. A discrete Gamma distribution was used to model the evolutionary rate differences among sites (5 categories (+G, parameter = 0.4657)). The tree is constructed to scale, with branch lengths measured in the number of substitutions per site. This analysis involved 10 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. There was a total of 503 positions in the final dataset. All of the above-mentioned analyses were conducted in MEGA X (Kumar et al., 2018).
ODV mapping software (Schlitzer, 2023) was employed to plot the geographical distribution of M. lauensis. The following abbreviations were used: CW - carapace width; min - minutes; P1, P2 - first and second pereopods; PCL - postorbital carapace length; s - seconds; SP2 - spade core 2; stn - station number.
SYSTEMATICS
Family Munidopsidae Ortmann, 1898
Genus Munidopsis Whiteaves, 1874
Munidopsis lauensis Baba and de Saint Laurent, 1992
Munidopsis lauensisBaba and de Saint Laurent, 1992: 326, fig. 3 (type locality: Valufa Ridge, Hine Hina, Lau Basin, BIOLAU 89, Nautile dive BL03, 22°32’S 176°43’E, 1,750 m). - Chevaldonné and Olu, 1996: 291. - Baba, 2005: 290 (key, synonymies). - Martin and Haney, 2005: 478, tabs 1, 2. - Macpherson and Segonzac, 2006: 443, figs. 1-3 . - Cubelio et al., 2007: 516, fig. 3. - Baba et al., 2008: 147 (synonymies). - Lin et al., 2013: 93, figs. 1, 2. - Thaler et al., 2014: fig. 1 (map). - Niu et al., 2017: fig. 6.5a (photograph). - Sun et al., 2019: record. - Hwang et al., 2022: fig. 1, tab. 1.
Material examined. 1 male (12.9 × 10.9 mm) (NIO1014/23), Krishna-Godavari Basin, western Bay of Bengal, off Machilipatnam, India, ORV Sindhu Sadhana, stn. SP3, 15°42.93726’N 82°03.82330’E, 1,754.9 m depth, spade corer, 18.III.2018, coll. M.J. Gonsalves.
Description of the present material. Body smooth (Fig. 2); carapace (Figs. 2, 3A, B) with PCL 1.2 ( CW, dorsal surface gently convex transversely. Rostrum triangular, length 0.4 times PCL, carinate dorsally, feebly upcurved, lateral margins finely serrated along distal one-third portion. Frontal margin strongly oblique; outer orbital spine represented by angular process. Gastric region dilated, bearing 1 pair of distinct anterior transverse striae. Anterior branchial region bearing short striae, anterolateral spine distinct, followed by few minute teeth. Slightly elevated submarginal ridge followed by gently concave posterior margin.
Thoracic sternum (Fig. 3C) smooth; sternite 3 posteriorly narrowed, anterior margin bearing 2 lobes, anterolateral angle terminating in distinct blunt process on each side. Pleon (Fig. 3D) smooth; tergites 2, 3 bearing 1 medially interrupted transverse groove each, that on tergite 2 distinct. Telson (Fig. 3E) comprising 10 plates.
Munidopsis lauensisBaba and Saint Laurent, 1992. Adult male PCL 12.9 mm, CW 10.9 mm (NIO1014/23). Dorsal habitus. Scale bar: 5 mm.
Ocular peduncle (Fig. 3 A , B) immovable, cornea ovate. First antennular peduncle article (Fig. 3 F ) unarmed on ventrodistal margin with, distolateral spine distinctly larger than distomesial spine. First antennal peduncle article (Fig. 3 F ) with distomesial spine reaching distal end of second article, distolateral spine short, not reaching distal end of second article; second article with short distolateral spine not reaching distal end of third article. Maxilliped 3 (Fig. 3 G ) ischium half as long as merus, distal angles prominent, crista dentata with 27 denticles; merus flexor margin with 2 small obsolescent spines, dorsal margin with small distolateral spine.
Munidopsis lauensisBaba and Saint Laurent, 1992. Adult male PCL 12.9 mm, CW 10.9 mm (NIO1014/23). A, Carapace dorsal view; B, carapace lateral view; C, thoracic sternum ventral view; D, pleonal tergites 1-5 dorsal view; E, pleonal tergite 6 and telson dorsal view; F, right antennule and antenna ventral view; G, third maxilliped lateral view; H, left P1 merus and carpus dorsal view; I, left P1 chela dorsal view; J, left P1 merus and carpus ventral view; K, left P1 chela ventral view; L, left P2 merus lateral view; M, Setae on extensor surface of left P2 merus; N, unattached pereopod ischium-propodus lateral view; O, unattached pereopod dactylus lateral view. Scale bars: A-E, H-M = 0.5 mm; N-O = 2 mm; F = 1 mm.
P1 (Figs. 2, 3 H -K) 1.8 ( PCL with long plumose setae. Ischium bearing distomesial spine. Merus with setose striae arranged longitudinally, distoventral and distomesial spines distinct, ventromesial margin bearing 3 spines. Carpus bearing mesial marginal spine at widest distal portion. Palm length 0.7 times finger length, almost as long as broad, mesially with 2 spiniform processes. Fingers distally spooned, occlusal margins crenulate.
P2 (Fig. 3 L ) merus with row of 9 small tuberculate spines (distalmost largest) on extensor surface, covered with rows of thick setae (Fig. 3 M ); lateral surface and ventral margin each with rows of obsolescent tubercular processes, flexor margin with distinct distal spine.
Pereopod (not attached to specimen) (Fig. 3 N ) merus 4.7 ( as long as wide, bearing dorsal row of 10 small spines, distalmost largest, lateral surface and ventral margin each bearing rows of obsolescent tubercular processes, ventral margin with distinct distal spine. Carpus with dorsal ridge terminating in distodorsal spine, feebly tuberculate low ridge dorsolaterally parallel to dorsal margin. Propodus obliquely flattish, dorsal margin bearing obsolescent tubercular processes. Dactylus (Fig. 3 O ) length 0.7 times propodus length, flexor margin bearing 17 teeth, each accompanied by movable corneous spine; distalmost tooth close to corneous unguis.
Epipods absent.
Distribution. Hydrothermal vents in the South-West Pacific at 1,750 m depth at Lau Basin near Fiji, 2,000 m in the North Fiji Basin (Baba and Saint Laurent, 1992; Thaler et al., 2014), 1,649 m at Brothers Seamount in the Kermadec Arc off New Zealand (Cubelio et al., 2007), 1,300-1,900 m at Manus Basin off Papua New Guinea (Thaler et al., 2014), and 2,023 m at Onnuri Vent Field in the Central Indian Ocean (Hwang et al., 2022).
Previous reports of M. lauensis from a cold-seep environment were from 1,119-1,199 m and 1,750-2,000 m at Formosa Ridge off Taiwan (Lin et al., 2013; Dong and Li, 2015; Shen et al., 2016; Yang et al., 2016; Sun et al., 2019).
Remarks. The morphology of the single Indian specimen of M. lauensis largely resembled the type specimens, with the exception of the higher number of teeth (27) on the crista dentata of the third maxilliped ischium (vs. 23-24 in the type series). Three males reported from the Formosa Ridge (Lin et al., 2013) reportedly possessed a relatively longer P1 palm (as long as finger), along with distinct spines on the mesial margin of P1 merus, which are less prominent in the Indian specimen, and absent in the type series.
The partial mtDNA COI sequence of the Indian specimen is identical (p-distance, 0.0%) (Tab. 2) to the previously published sequences originating from the Northwestern Pacific Ocean (KF774316 (Lin et al., 2013), and MH717895 (Sun et al., 2019)) (Fig. 4). The partial 16S rRNA sequence is nearly identical (p-distance, 1.25%) to the previously published sequence (MH717895) from the Formosa Ridge, Taiwan (Sun et al., 2019).
Kimura 2 parameter (K2P) pair-wise analysis based estimated genetic variation among COI sequences of species of Munidopsis.
Maximum Likelihood (ML) tree showing relationships among MunidopsisWhiteaves, 1874 species based on COI gene sequence data. Numbers on branches represent bootstrap values expressed in percentages.
Munidopsis lauensis belongs to the “orophorhynchus” species group of the genus Munidopsis, characterized by a mesially placed distal eye-spine, and chelipeds shorter in length than the second pereopods. This group also includes 18 other congeneric species reported from the Atlantic, Indo-Pacific and Southern Oceans (Tab. 3). Within the “orophorhynchus” species group, M. lauensis shares the absence of epipods from all the pereopods with Munidopsis albatrossaePequegnat and Pequegnat, 1973, Munidopsis aries (A. Milne-Edwards, 1880), Munidopsis arietinaAlcock and Anderson, 1894, Munidopsis centrinaAlcock and Anderson, 1894, Munidopsis ceratophthalmaAlcock, 1901, Munidopsis granosaAlcock, 1901, Munidopsis platirostris (A. Milne-Edwards and Bouvier, 1894), Munidopsis sharreri (A. Milne-Edwards, 1880), and Munidopsis spinoculata (A. Milne-Edwards, 1880). It differs from M. arietina, M. granosa, and M. platirostris in having a narrow triangular rostrum; from M. sharreri in the smooth posterior margin of the carapace; from M. albatrossae in possessing moderately arched lateral carapace margins; from M. aries and M. centrina in the absence of gastric spines on the carapace; and from M. spinoculata in the presence of spines on the meri and carpi of pereopods. It closely resembles M. ceratophthalma in possessing a narrow triangular rostrum, absence of gastric spines, moderately arched lateral carapace margins, smooth posterior margin of carapace, the presence of spines on the meri and carpi of pereopods, and absence of epipods on all pereopods. However, M. lauensis differs from M. ceratophthalma in having a relatively shorter mesial eye-spine, which is less than half of the rostral length (vs. relatively longer eye-spine, greater than half of the rostral length in M. ceratophthalma). An identification key to the species of the “orophorhynchus” group is provided below.
Geographical and bathymetric distribution of species belonging to the “orophorhynchus” species group of the genus MunidopsisWhiteaves, 1874.
Identification key to the species of the “orophorhynchus” group of the genus Munidopsis:
1. Epipods absent on chelipeds and pereopods…………………………………..………….. 2
- Epipods present on chelipeds, may be absent on pereopods.............................................. 11
2. Rostrum styliform, bearing lateral spines……….……………………………… M. arietina
Rostrum narrowly to broadly triangular, unarmed laterally……………………….……… 3
3. Rostrum broadly triangular ……………………………………………………….………. 4
Rostrum narrowly triangular……………………..……………………………….…….…. 5
4. Carapace uniformly tuberculate. Abdominal somites 2-4 each with sharp median tooth…………………………………………………………….......................... M. granosa
Carapace sparsely tuberculate. Abdominal somites 2-4 unarmed…………… M. platirostris
5. Posterior margin of carapace spinose………..………………………………..…. M. sharreri
Posterior margin of carapace smooth………………………………….……..…………….. 6
6. Carapace broadest anteriorly, lateral margins converging posteriorly…….… M. albatrossae
Carapace broadest at midlength, lateral margins moderately arched…………..…………… 7
7. Carapace with gastric spines……………………………..………………………………….. 8
Carapace without spines on the gastric region…………………………………………….… 9
8. Carapace with 1 pair of gastric spines…….………………………………………….. M. aries
Carapace with 2 transverse rows of gastric spines………………………………... M. centrina
9. Surfaces of meri and carpi of chelipeds and pereopods armed with spines or tubercles........ 10
Surfaces of meri and carpi of chelipeds and pereopods unarmed……...……… M. spinoculata
10. Eye-spine longer than half of rostral length………………………...…….. M. ceratophthalma
Eye-spine shorter than half of rostral length………………………………………. M. lauensis
11. Epipods present on chelipeds and first two ambulatory pereopods ……………………………
……..…...…………….……………………………… M. marionis (A. Milne-Edwards, 1882)
Epipods present on chelipeds only…………………………………….……………..………12
12. Rostrum broadly triangular…………………………………………..………………………13
Rostrum moderately triangular………………………………..…………..…………….……16
13. Carapace with 1 pair of gastric spines……………………..………… M. pallidaAlcock, 1894
Carapace without gastric spines……………………………………………….……………. 14
14. Abdominal somites 2-4 each with blunt, low median process……... M. parfaiti (Filhol, 1885)
Abdominal somites 2-4 unarmed……………………………….…….…………………….. 15
15. Dorsal surface of carapace nearly smooth. Rostrum constricted between eyes……………..…
……………………………………………………………………….. M. livida (Perrier, 1886)
Dorsal surface of carapace sharply granulated. Rostrum not constricted between eyes……...
……………………………………….…………….. M. squamosa (A. Milne-Edwards, 1880)
16. Carapace with spines on gastric region…………………..………………… ………………17
Carapace without spines on gastric region………………………………………………..…….
………………………………. M. edwardsi (Wood-Mason in Wood-Mason & Alcock, 1891)
17. Carapace with 1 pair of spines only on gastric region………………………………….………
…………………………………………………………... M. nitida (A. Milne-Edwards, 1880)
Carapace with spines in addition to 1 pair of spines on gastric region………………...…… 18
18. P2-4 dactyli nearly straight on flexor margin………….……….….……. M. rectaBaba, 2005
P2-4 dactyli considerably curving……………..……….… M. subsquamosaHenderson, 1885
DISCUSSION
Morphological and molecular (partial mitochondrial cytochrome oxidase subunit 1 and 16S rRNA genes) analyses of deep-water squat lobsters collected from a cold-seep site in the western Bay of Bengal confirmed the first geographical record of Munidopsis lauensis from Indian waters. The present study was a preliminary attempt to shed light on the squat lobster fauna of the cold seep environment in the Northern Indian Ocean. Additional sampling surveys are required to fully understand the species composition of this little-studied region.
ACKNOWLEDGEMENTS
The first author gratefully acknowledges the Director CSIR-NIO for the support and facilities. Ms. Nitisha Sangodkar and Ms. Delcy Nazareth are acknowledged for their assistance onboard and in the laboratory. The second author acknowledges the funding from the Ministry of Earth Sciences Research Fellowship Program (MRFP) for carrying out this study. The manuscript benefited from the suggestions of the anonymous referees. This is NIO contribution no. 7272.
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Consent for publication
All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document.
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Funding and grant disclosures
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Not relevant.
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Study permits
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Zoobank:
http://zoobank.org/urn:lsid:zoobank.org:pub:86DA04AA-7D6C-4397-B1B8-427A39563A7C
Publication Dates
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Publication in this collection
03 Feb 2025 -
Date of issue
2025
History
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Received
18 Jan 2024 -
Accepted
13 June 2024
