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Review
. 2011 Feb 14;6(2):e16309.
doi: 10.1371/journal.pone.0016309.

New perspectives on the ecology and evolution of siboglinid tubeworms

Affiliations
Review

New perspectives on the ecology and evolution of siboglinid tubeworms

Ana Hilário et al. PLoS One. .
No abstract available

PubMed Disclaimer

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Citation counts for papers published in the journals Nature or Science.
Cumulative citation count for papers published in over the years 1958 to 2007 that deal exclusively with species in the annelid clade Siboglinidae (papers covering general vent/seep biology or symbiosis in general are not included). Significant discoveries are highlighted by arrows and major increases in total citations. These include discoveries in feeding , the discovery of bacterial symbiosis , sulfide binding , tubeworms at shipwrecks , respiration , embryology , larval dispersal and the new clade of siboglinids (Osedax) that consume whale bones .
Figure 2
Figure 2. Examples of siboglinid species and their habitat requirements.
A) Riftia pachyptila giant tubeworms growing on a hydrothermal vent in the north-east Pacific (Image courtesy of Richard Lutz), B) Lamellibrachia luymesi at a cold seep in the Gulf of Mexico (Image courtesy of DT, KH, Kevin Fielman and Scott Santos) and C) Osedax mucofloris living on a whale-bone found off the coast of Sweden.
Figure 3
Figure 3. Phylogenetic relationships amongst Siboglinidae.
A Bayesian analysis of 18S ribosomal RNA sequences reveals four major clades of siboglinids, from top, Osedax which are specialist on whale carcasses, the vestimentiferans, which are specialist on vents and seeps, Sclerolinum (here presented only by a single sequenced specimen), specialist on organic-rich remains and the frenulates which specialise on organic-rich sediments. Modified from . Images courtesy of Tomas Lundälv (whale-fall), Richard Lutz (vent site) and NOCS/JC10 (frenulate in sediment).
Figure 4
Figure 4. Cumulative number of species descriptions since the discovery of the first siboglind.
With the exception of Sclerolinum, the curve does not asymptote showing that new species have been (up to this day) continuously disclosed.
Figure 5
Figure 5. Tube fossils possibly attributable to vestimentiferans.
Tube fossils from ancient seep and vent deposits possibly attributable to vestimentiferans and modern vestimentiferan tubes for comparison. A) Cluster of pyrite replaced tubes in matrix of pyrite, Kambia vent deposit, Cyprus, Early Cretaceous (91 Ma). B) Pyrite replaced tube in pyrite matrix, Figueroa vent deposit, California, USA, Early Jurassic (∼184 Ma), note fine concentric growth lines and wavy, periodically bifurcating longitudinal ridges. C) Tube of holotype (NHM1996:1048) of vestimentiferan Arcovestia ivanovi, note external ornament of fine concentric growth lines and wavy, periodically bifurcating longitudinal ridges. D) Carbonate tubes in matrix of carbonate minerals, Canyon River seep deposit, Washington, USA, Oligocene (∼30 Ma), specimen courtesy of James Goedert. E) Carbonate replaced tube of vestimentiferan (probably Escarpia southwardae) in transverse section from modern seep in the Kouilou pockmark field on the Congo deep-sea fan, 3100m water depth. The original organic tube has been ‘delaminated’ by the growth of aragonite crystals within it. F) Carbonate tube in transverse section, Ganigobis seep deposits, Namibia, Late Carboniferous (∼302 Ma), showing very similar textures to the tube in E. Scale bars: A = 10mm, B = 1mm, C = 2mm, D = 10mm, E = 100µm, F = 100µm.
Figure 6
Figure 6. Sources of sulphide and respiratory pathways at contrasting habitats in siboglinid tubeworms.
At hydrothermal vents, sulphide is produced through the inorganic reaction of sulphate with geothermal energy. By contrast, sulphide has a microbial origin at cold seeps, organic-rich sediments, and whale-falls. At cold seeps, the source of sulphide is the anaerobic oxidation of methane coupled to sulphate reduction. At organic-rich sediments, sulphide is produced during the anaerobic degradation of a range of organic compounds. At whale-falls, although sulphide is produced, Osedax worms are thought to rely only on heterotrophic digestion of bone by the endosymbionts. The trophosome (light grey) houses endosymbiotic bacteria (orange ovals). White open circles represent methane and hydrocarbon seepage. Full arrow = reaction, dashed arrow = diffusion, and dotted arrow = acquisition or excretion by the host/symbiont.
Figure 7
Figure 7. Life-history traits of Vestimentifera, Osedax and Frenulata.
A) Histological section through the spermatheca of Riftia pachyptila (Vestimentifera) (Gc = Gonocoel, PO = Primary oocyte, S = Clusters of spermatozoa, St = Spermatheca) (from [135]). B) Two live males on the trunk of a female of an undescribed species of Osedax recovered in Antarctic waters. C) Brooding larva inside the tube of Siboglinum sp. (Frenulata). Scale bars: A = 200 µm, B = 100 µm, C = 500 µm.
Figure 8
Figure 8. An evolutionary scenario for the origin of the major siboglinid clades and their respective symbiont.
Note that the sister-group relationship between Osedax and the vestimentiferan-Sclerolinum clade is currently only weakly supported. In this scenario, the putative siboglinid ancestor possessed chemoautotrophic symbionts that have been secondarily lost in Osedax and replaced by a heterotrophic symbiont. Images courtesy of DT, KH, Kevin Fielman and Scott Santos (vestimentiferan), Irmgard Eichinger (Sclerolinum).

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