On the presence of the deep-sea blind lobster Stereomastis suhmi (Decapoda: Polychelidae) in Southwestern Atlantic waters and its circum-Antarctic distribution

Abstract

Here we report on the presence of the deep-sea blind lobster Stereomastis suhmi in the Southwestern Atlantic. The species identification was based on morphological traits and confirmed with genetic barcoding. The specimen analysed shows little difference from previous descriptions. This work extends the range of S. suhmi in America, where it was previously limited to the Pacific coasts off Chile, to the mouth of the Rio de la Plata, Argentina, and confirms its circumpolar presence with molecular data. A review of all available records shows that the overall distribution of the species is well correlated with the presence of Antarctic Intermediate Waters suggesting that the species habitat is restricted to cold and relatively low-salinity/oxygen-rich waters.

Keywords:

• Argentina
• barcoding
• Crustacea
• deep-sea
• new record

Introduction

Polychelidan lobsters are noticeable among reptant decapods in having chelae on almost all pereopods (always on pereopods 1–4, but sometimes also on pereopod 5). The most recent phylogenetic analyses depict polychelidan lobsters as basal in the Reptantia, recognising a separate infra-ordinal status for the polychelidans (Ahyong 2009; Bracken-Grissom et al. 2014) with four families, from which only one, the Polychelidae Wood-Mason, 1875, is extant. Although evolved from shallow-water forms, extant Polychelidae have strongly reduced eyes, are confined to deep water, and are therefore known as ‘deep-sea blind lobsters’. Modern polychelids display burrowing habits (Gore 1984) and are scavengers and detritus feeders, although they appear to be also ambush predators, particularly of small epibenthic crustaceans (Cartes & Abello 1992). To date, Polychelidae contains six genera and 38 species worldwide (Chan 2010), of which only four species in three genera have been recorded from the southwestern Atlantic, all from Brazilian waters: Pentacheles laevis Bate 1878; Pentacheles validus A. Milne Edwards 1880; Polycheles typhlops Heller 1862 (Dall’Occo & Tavares 2004); and Stereomastis sculpta Smith 1880 (Ramos-Porto et al. 2000; mentioned as [Polycheles sculptus] in Dall’Occo & Tavares 2004).

Recently the RV Puerto Deseado, belonging to CONICET, started a series of expeditions extensively surveying the Argentinian marine fauna, particularly deep-sea areas that remained largely unexplored. As part of this programme, during September 2013 the campaign ‘Talud III’ was carried out with the specific aim of exploring the Mar del Plata Canyon, located off Mar del Plata (around 37.5°S, 54°W), Argentina. This submarine canyon is a perpendicular cut of the continental slope starting at 500-m depth that becomes V-shaped between 1200 and 3700 m, and finally opens to connect the continental shelf with the abyssal plains (Violante et al. 2010). Here we report the first record of the deep-sea blind lobster Stereomastis suhmi (Bate 1878), in the southwestern Atlantic, and discuss this new finding in the framework of the general distribution of the species and the related oceanographic features.

Materials and methods

During the ‘Talud III’ cruises of the RV Puerto Deseado, a total of 28 hauls were performed (16 with an otter bottom trawl net with 6-m headrope, 10-mm mesh size at the cod end; and 12 with a small epibenthic dredge with 0.6-m horizontal opening, 5-mm mesh size) between 774 m and 3320 m depth. The specimen of S. suhmi was collected with the bottom trawl, photographed immediately after it came on board and preserved in 96% ethanol. The carapace length (CL) was measured to the nearest 0.1 mm dorsally along the midline, from the base of the rostrum to the posterior margin of the carapace.

Species identification was based on morphology, following the keys and terminology in Bate’s original description (Bate 1878) and Galil (2000) and Ahyong (2009). To corroborate the species identification, a tissue sample was obtained from the abdomen of the specimen and used for molecular analysis of a partial fragment of the barcode gene cytochrome c oxidase subunit I (COI). DNA extraction, polymerase chain reaction amplification, polymerase chain reaction product purification and sequencing were conducted following the protocols of the Canadian Centre for DNA Barcoding (CCDB protocols http://ccdb.ca/resources.php; see also Ivanova et al. 2006), using the universal primers HCO2198 (5′-TAA ACT TCA GGG TGA CCA AAA AAT CA-3′), and LCO1490 (5′-GGT CAA CAA ATC ATA AAG ATA TTGG-3′). Identification was performed using standard nucleotide BLAST^® (http://blast.ncbi.nlm.nih.gov/Blast.cgi) to search in the Barcode of Life (BOLD, http://www.boldsystems.org/) and GenBank (www.ncbi.nlm.nih.gov/GenBank) databases. The voucher specimen was deposited at the Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Argentina under the catalogue number MACN-In 39629. The COI sequence obtained is available on GenBank under accession number KM503116, as well as in the ‘Native and exotic invertebrate of Mar del Plata harbour’ project (code INVMP) on the BOLD system.

Results

Material examined

One male S. suhmi (Fig. 1), CL 15.7 mm, (right chela is missing), Mar del Plata Canyon, continental slope of Argentina, southwest Atlantic, 38°072′S, 54°123′W, 1800 m depth, 7 September 2013, MACN-In 39629.

Figure 1 Dorsal and lateral view of a male Stereomastis suhmi, carapace length 15.7 mm, captured in the Mar del Plata Canyon, continental slope of Argentina, southwest Atlantic, 38°072′S, 54°123′W, at 1800 m depth, MACN-In 39629.

Morphological diagnosis and molecular identification

Carapace distinctly longer than wide; dorsal orbital notch U-shaped; median carina on abdominal tergites 2–5 with a short, upright posterior tooth in addition to strong antrorse spine; inner angle of dorsal orbital sinus spinose (Figs 1–2). Examined but not shown in figures: epipod of pereopods 1–5 vestigial; dactylus and pollex of pereopods straight; outer proximal margin of basal antennular segment with two spines; ischium and merus of pereopod 2 articulated.

Figure 2 Stereomastis suhmi (Bate 1878): Comparison of previously described specimens with the one reported in this work. A, B, Dorsal view of the cephalothorax. A, Female 31.2 mm, off Cape Province, ‘Africana’, 31°20′S, 16°09′E, 462 m (from Galil 2000). B, Male of S. suhmi, carapace length 15.7 mm in this work, MACN-In 39629. C, D, Lateral view of the abdomen. C, Female 26.5 mm, Tasman Sea, ‘Galathea’ stn 626, 42°10′S, 170°10′E, 610 m. D, Male of S. suhmi, carapace length 15.7 mm in this work, MACN-In 39629. Pictures of previously described specimens are from Galil (2000), © Publications Scientifiques du Muséum National D’histoire Naturelle, 21:285–387.

The 658 nucleotides of COI sequence obtained from our specimen showed 99% similarity with the mitochondrial COI sequence of an S. suhmi collected by RV Tangaora in Campbell Plateau, New Zealand (48°45′S, 172°036′E; 700 m depth) and published in GenBank (accession number: KF828018.1). It also matched (100% similarity) a sequence of another specimen of S. suhmi available on the BOLD system, also from southeast of New Zealand, confirming that the Argentine specimen and the previously sequenced specimens are conspecific.

Remarks

This specimen shows little difference with Bate’s (1878) original description of S. suhmi and further descriptions elsewhere (Galil 2000; Ahyong 2009). In general all spines seem blunt and smaller than in previous descriptions (Griffin & Stoddart 1995; Galil 2000) and particularly the spines of the anterolateral angle of the carapace and those posterior to the post-cervical incision, appear to be more upwardly curved (see Fig. 2). A similar pattern was described in at least one individual from off southern Africa (figure 9 in Calman 1925). Spines in the branchial carina are less conspicuous, low and smooth than previous descriptions. In all other respects this specimen is a typical S. suhmi. There are two rostral spines plus a smaller spine on the internal orbital angle. The orbital sinus is smooth, subtriangular and deep; there is no spine at the external orbital angle. The spinal formula of the lateral edge of the carapace is 5:2:8.

Discussion

The present work extends the range of S. suhmi in America, from the Pacific coasts off Chile and archipelago of Tierra del Fuego (Bate 1878; Arntz et al. 1999; Boschi & Gavio 2005), to the southwestern Atlantic, reaching north to almost the mouth of the Rio de la Plata (36°S). Hence, the species is expected to be present along the entire Magellanic Biogeographic Province, which encompasses the coasts from northern Chiloé Island on the eastern Pacific to the southwestern Atlantic waters, off the continent at 43°S, stretching north to reach 35°S (Fig. 3) (Boschi & Gavio 2005).

Figure 3 Schematic representation of the distribution of Stereomastis suhmi and oceanographic features mentioned in the text. The dark star corresponds to the location of the new record reported in this work. Dark areas in continental margins are the previously known distribution. The grey transparent shaded area marked by the dotted line between the new record and those from Chilean Patagonia and Magellan’s Strait represents the hypothetical Magellanic distribution of the species in America. The area of formation of Antarctic Intermediate Water (AAIW) and the branches flowing towards the equator are in light grey, dotted lines and double-headed arrows. Dashed lines with simple-headed arrows are main surface currents. STF, Subtropical front (or subtropical convergence); SAF, Subantarctic front; PF, Polar front (also known as Antarctic convergence).

Stereomastis suhmi was recorded at depths ranging from 200 to 2200 m in southeastern Atlantic Ocean (western coast of South Africa), western Pacific Ocean (south-eastern Australia and New Zealand), and south-eastern Pacific Ocean (south-western coast of South America, west coast of Patagonia of Chile) (Calman 1925; Griffin & Stoddart 1995; Galil 2000; Ahyong 2012). To date the southernmost record of S. suhmi (larvae or adults) has been from the Pacific portion of the Magellanic region, south of the Beagle Channel around 2100 m depth on the continental slope (Arntz et al. 1999; Thatje et al. 2003). Although it was suggested that adult S. suhmi may occur in the deep of the Drake Passage and even further south (Thatje & Arntz 2004), recent polychelid lobsters are virtually absent south of the Polar front (Gorny 1999; Thatje & Arntz 2004; Griffiths et al. 2013). The only exception to date is a record of five mesopelagic larvae of S. suhmi found close to South Georgia Island, between 400 and 800 m depth (Tiefenbacher 1994).

Current records of S. suhmi fall mostly within the so-called antiboreal or transitional region (Gorny 1999), which is located between the Subtropical and Polar fronts (Orsi et al. 1995; also known as the Subtropical and Antarctic Convergences respectively) depicting a rather circumpolar distribution (Fig. 3). Nevertheless, circumstantial records of adult S. suhmi far north of the Subtropical front in waters off West Africa (in the Cameroon volcanic line at c.3°S–3°E; Ocean Biogeographic Information System challenge this idea. (Specimen collected by the South Atlantic MAR-ECO 2009 cruise EurOBIS. The record is published in the Ocean Biogeographic Information System with an error in the collection depth, which is actually 997 m. Both the species ID and collection depth were confirmed by Dr Irene A. Cardoso in a personal communication to NEF.) The virtual absence of the species in areas where one would expect it to be based solely on a continuous circumpolar distribution (e.g. southeastearn Africa) also challenges this idea.

Because the species is clearly limited to deep bottoms, an explanation of its current geographic distribution requires taking into account the circulation pattern of the deep water masses, which has proved to be the main explanatory factor for the diversity and biomass of deep-sea decapods (e.g. Cartes et al. 2014 and references therein). At the depth range and areas inhabited by adult S. suhmi and their larvae (Thatje et al. 2003) the predominant oceanographic feature is the presence of the cold and relative low-salinity/oxygen-rich Antarctic Intermediate Water (AAIW) formed in the Antarctic Convergence zone, where it sinks and is distributed into all ocean basins, to lastly spread northward, filling most of the world’s ocean at intermediate depths (c.1000 m) (Talley 1999). Branches of AAIW that flow towards the equator, carry cold and relatively fresh subantarctic water that can be identified in intermediate waters as far north as 20°N, with trace amounts as far as 60°N (Talley 1999). The new record for S. suhmi reported here occurred precisely within the northern limit of the Malvinas Current, which transports subantarctic waters northwards and extends all the way to the sea-floor (Boschi & Gavio 2005). Similarly, the record of S. suhmi close to the equator off West Africa, may be explained also by the presence of a branch of AAIW that stretches northeast along the African slope, reaching as far north as the Canary Archipelago (28°N) (Machín & Pelegrí 2009). In both cases many hauls were performed with different sampling gear but only one specimen was collected. The seeming rarity of the species at these two locations should not be surprising considering that both records are at the limits of AAIW branches, i.e. at the periphery of the supposed species optimal distribution.

On the other hand, the absence of S. suhmi in well-explored, deep-sea areas (where other Polychelidae are commonly found) also supports a species distribution influenced by the presence of AAIW. For example, explorations in the southern continental slope of Brazil found many polychelidan species other than S. suhmi (Ramos-Porto et al. 2000; Dall’Occo & Tavares 2004), indicating that the species does not extend north beyond the influence of the Malvinas Current. In turn, the absence of S. suhmi off East Africa supports the association of S. suhmi with cold AAIW because the Agulhas Current blocks the eastward penetration of AAIW from the Atlantic (Piola & Georgi 1982). In summary, the current distribution of S. suhmi appears strongly correlated with the presence of intermediate subantarctic waters, suggesting that the species is restricted to cold and relative low-salinity/oxygen-rich waters.

Associate Editor: Dr Jonathon Banks.

Acknowledgements

We want to acknowledge the crew of the RV Puerto Deseado and colleagues for their assistance during the cruise. We are grateful for the support provided by the Government of Canada through Genome Canada and the Ontario Genomics Institute to the International Barcode of Life Project. This funding enabled the Canadian Centre for DNA Barcoding (University of Guelph) to carry out the sequence analysis on our specimen. We also thank the Ontario Ministry of Economic Development and Innovation for funding the ongoing development of BOLD. The present work was supported by PIP 830/ 2012 (CONICET—Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina) and EXA 618/12 (UNMdP—Universidad Nacional de Mar del Plata, Argentina). NEF was also supported by CONICET through a postdoctoral fellowship. Lastly, we want to thank the two anonymous referees for their helpful suggestions and comments.