Hostname: page-component-5db58dd55d-688nx Total loading time: 0 Render date: 2026-05-31T15:50:57.432Z Has data issue: false hasContentIssue false
  • English
  • Français

Systematics, functional morphology and distribution of a bivalve (Apachecorbula muriatica gen. et sp. nov.) from the rim of the ‘Valdivia Deep’ brine pool in the Red Sea

Published online by Cambridge University Press:  11 November 2014

P. Graham Oliver ,
Hege Vestheim ,
André Antunes  and
Stein Kaartvedt
P. Graham Oliver*
Affiliation:
National Museum of Wales, Cathays Pk., Cardiff CF10 3NP, Wales, UK
Hege Vestheim
Affiliation:
King Abdullah University of Science and Technology, Red Sea Research Center, Thuwal 23955–6900, Saudi Arabia
André Antunes
Affiliation:
IBB – Institute for Biotechnology and Bioengineering, Centre of Biological Engineering, Micoteca da Universidade do Minho, University of Minho, Braga, Portugal
Stein Kaartvedt
Affiliation:
King Abdullah University of Science and Technology, Red Sea Research Center, Thuwal 23955–6900, Saudi Arabia
*
Correspondence should be addressed to: P.G. Oliver, National Museum of Wales, Cathays Pk., Cardiff CF10 3NP, Wales, UK email: graham.oliver@museumwales.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

The deep brine pools of the Red Sea comprise extreme, inhospitable habitats yet house microbial communities that potentially may fuel adjacent fauna. We here describe a novel bivalve from a deep-sea (1525 m) brine pool in the Red Sea, where conditions of high salinity, lowered pH, partial anoxia and high temperatures are prevalent. Remotely operated vehicle (ROV) footage showed that the bivalves were present in a narrow (20 cm) band along the rim of the brine pool, suggesting that it is not only tolerant of such extreme conditions but is also limited to them. The bivalve is a member of the Corbulidae and named Apachecorbula muriatica gen. et sp. nov. The shell is atypical of the family in being modioliform and thin. The semi-infaunal habit is seen in ROV images and reflected in the anatomy by the lack of siphons. The ctenidia are large and typical of a suspension feeding bivalve, but the absence of ‘guard cilia’ and the greatly reduced labial palps suggest that it is non-selective as a response to low food availability. It is proposed that the low body mass observed is a consequence of the extreme habitat and low food availability. It is postulated that the observed morphology of Apachecorbula is a result of paedomorphosis driven by the effects of the extreme environment on growth but is in part mitigated by the absence of high predation pressures.

Keywords

Corbulidaedeep-hyper-saline anoxic basins (DHABs)Red Seadeep-seaApachecorbula gen. nov.functional morphologyValdivia Deepdeep-sea bivalves

Information

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 3 , May 2015 , pp. 523 - 535
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

Allen, J.A. (1979) The adaptations and radiation of deep-sea bivalves. Sarsia 64, 19–27.Google Scholar
Allen, J.A. (2008) Bivalvia of the Deep Atlantic. Malacologia 50, 57–173.Google Scholar
Anderson, L.C. and Roopnarine, P.D. (2003) Evolution and phylogenetic relationships of Neogene Corbulidae (Bivalvia: Myoidea) of tropical America. Journal of Paleontology 77, 1086–1102.Google Scholar
Anisimova, M. and Gascuel, O. (2006) Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Systematic Biology 55, 539–552.Google Scholar
Antunes, A., Ngugi, D.K. and Stingl, U. (2011) Microbiology of the Red Sea (and other) deep-sea anoxic brine lakes. Environmental Microbiology Reports 3, 416–433.Google Scholar
Batang, Z.B., Papathanassiou, E., Al-Suwailem, A., Smith, C., Salomidi, M., Petihakis, G., Alikunhi, N.M., Smith, L., Mallon, F., Yapici, T. and Fayad, N. (2012) First discovery of a cold seep on the continental margin of the central Red Sea. Journal of Marine Systems 94, 247–253.Google Scholar
Bischoff, J.L. (1969) Red Sea geothermal brines deposits: their mineralogy, chemistry and genesis. In Degens, D.T. and Ross, D.A. (eds) Hot brines and recent heavy metal deposits in the Red Sea. New York, NY: Springer Verlag, pp. 308–401.Google Scholar
Braithwaite, C.J.R. (1987) Geology and paleogeography of the Red Sea region. In Edwards, A.J. and Head, S.M. (eds) Key environments: the Red Sea. Oxford: Pergamon Press, pp. 22–44.Google Scholar
Brown, R.W. (1956) Composition of scientific words. London: Smithsonian Institution Press, 882 pp.Google Scholar
Carney, S.L., Formica, M.I., Divatia, H., Nelson, K., Fisher, C.R. and Schaeffer, S.W. (2006) Population structure of the mussel “Bathymodiolus” childressi from Gulf of Mexico hydrocarbon seeps. Deep Sea Research Part I 53, 1061–1072. http://dx.doi.org/10.1016/j.dsr.2006.03.002.Google Scholar
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.Google Scholar
Chevenet, F., Brun, C., Banuls, A.L., Jacq, B. and Christen, R. (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7, 439.Google Scholar
Cordes, E.E., Hourdez, S. and Roberts, H.H. (2010) Unusual habitats and organisms associated with the cold seeps of the Gulf of Mexico. In Kiel, S. (ed.) The vent and seep biota: aspects from microbes to ecosystems. Topics in geobiology, Vol. 33. Berlin: Springer, pp. 315–332.Google Scholar
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.F., Guindon, S., Lefort, V., Lescot, M., Claverie, J.M. and Gascuel, O. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 1, 36.Google Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Giribet, G., Carranza, S., Baguñà, J., Riutort, M. and Ribera, C. (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76–84.CrossRefGoogle ScholarPubMed
Grill, B. and Zuschin, M. (2001) Modern shallow- to deep-water bivalve death assemblages in the Red Sea ecology and biogeography. Palaeogeography, Palaeoclimatology, Palaeoecology 168, 75–96.Google Scholar
Guindon, S. and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Gustafson, R.G., Turner, R.D., Lutz, R.A. and Vrijenhoek, R.C. (1998) A new genus and five new species of mussels (Bivalvia: Mytilidae) from deep-sea sulfide/hydrocarbon seeps in the Gulf of Mexico. Malacologia 40, 63–112.Google Scholar
Hallan, A., Colgan, D.J., Anderson, L.C., García, A. and Chivas, A.R.A. (2013) A single origin for the limnetic–euryhaline taxa in the Corbulidae (Bivalvia). Zoologica Scripta 42, 278–287.Google Scholar
Hartmann, M. (1985) Atlantis II deep geothermal brine system. Chemical processes between hydrothermal brines and Red Sea deep water. Marine Geology 64, 157–177.Google Scholar
Hayami, I. and Kase, T. (1993) Submarine cave bivalvia from the Ryukyu Islands: systematics and evolutionary significance. The University Museum, The University of Tokyo, Bulletin 35, 1–133.Google Scholar
Lampadariou, N., Hatziyanni, E. and Tselepides, A. (2003) Community structure of meiofauna and macrofauna in Mediterranean deep-hyper-saline anoxic basins: CIESM, 2003. Mare Incognitum? Exploring Mediterranean deep-sea biology. CIESM Workshop Monographs no 23, 128 pages, Monaco. www.ciesm.org/publications/Heraklion03.pdf.Google Scholar
Lorion, J., Buge, B., Cruaud, C. and Samadi, S. (2010) New insights into diversity and evolution of deep-sea Mytilidae (Mollusca: Bivalvia). Molecular Phylogenetics and Evolution 57, 71–83.Google Scholar
MacDonald, I.R., Guinasso, H.L., Reilly Brooks, J.M., Callender, W.R. and Gabrielle, S.G. (1990) Gulf of Mexico hydrocarbon seep communities. VI. Patterns in community structure and habitat. Geo-Marine Letters 10, 244–252.Google Scholar
Melvill, J.C. and Standen, R. (1907) The Mollusca of the Persian Gulf, Gulf of Oman and Arabian Sea, as evidenced mainly through the collections of Mr. F. W. Townsend, 1893–1906; with descriptions of new species. Part II. – Pelecypoda. Proceedings of the Zoological Society of London 1906, 783–848.Google Scholar
Mikkelsen, P.M. and Bieler, R. (2001) Varicorbula (Bivalvia: Corbulidae) of the western Atlantic: taxonomy, anatomy, life habits, and distribution. The Veliger 44, 271–293.Google Scholar
Morton, B. (1990) The biology and functional morphology of Corbula crassa (Bivalvia: Corbulidae) with special reference to shell structure and formation. In Morton, B. (ed.) The marine flora and fauna of Hong Kong and Southern China II. Volume 3. Behaviour, morphology, physiology and pollution. Hong Kong: Hong Kong University Press, pp. 1055–1073.Google Scholar
Ockelmann, K.W. (1964) Turtonia minuta (Fabricius), A neotenous veneracean bivalve. Ophelia 1, 121–146.Google Scholar
Oliver, P.G. (1979) Adaptations of some deep-sea suspension feeding bivalves (Limopsis and Bathyarca). Sarsia 64, 33–36.Google Scholar
Oliver, P.G. (1992) The Bivalve Seashells of the Red Sea. An Identification Guide. Christa Hemmen Verlag, Wiesbaden & The National Museum of Wales, Cardiff. 330pp., 46 col. pls.Google Scholar
Oliver, P.G. (2001) Functional morphology and description of a new species of Amygdalum (Mytiloidea) from the oxygen minimum zone of the Arabian Sea. Journal of Molluscan Studies 67, 225–241.Google Scholar
Salas, C. (1994) Notolimea clandestina a new species of neotenous bivalve (Bivalvia: Limidae) endemic to the Strait of Gibraltar. Journal of Molluscan Studies 63, 249–254.Google Scholar
Taylor, J.D. and Glover, E.A. (2010) Chemosymbiotic bivalves. In Kiel, S. (ed.) The vent and seep biota: aspects from microbes to ecosystems. Topics in geobiology, Vol. 33. Berlin: Springer, pp. 107–135.Google Scholar
Türkay, M. (1996) Composition of the deep Red Sea macro- and megabenthic invertebrate fauna. Zoogeographic and ecological implications. In Uiblein, F., Ott, J. and Stachowitsch, M. (eds) Deep-sea and extreme shallow-water habitats: affinities and adaptations. Biosystematics and ecology, Series 11. Vienna: Austrian Academy of Sciences, pp. 43–59.Google Scholar
Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. and Wheeler, W.C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.Google Scholar
Xiong, B. and Kocher, T.D. (1991) Comparison of mitochondrial DNA sequences of seven morphospecies of black flies (Diptera: Simuliidae). Genome 34, 306–311.Google Scholar
Yonge, C.M. (1946) On the habits and adaptations of Aloidis (Corbula) gibba. Journal of the Marine Biological Association of the United Kingdom 26, 358–376.Google Scholar
Zierenberg, R.A. and Shanks, W.C. III (1986) Isotopic constraints on the origin of the Atlantis II, Suakin and Valdivia brines, Red Sea. Geochimica et Cosmochimica Acta 50, 2205–2214.Google Scholar