Serpulids Living Deep Calcareous Tubeworms Beyond the Abyss
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Deep-Sea Research I 90 (2014) 91–104 Contents lists available at ScienceDirect Deep-Sea Research I journal homepage: www.elsevier.com/locate/dsri Serpulids living deep: calcareous tubeworms beyond the abyss$ Elena K. Kupriyanova a,n, Olev Vinn b, Paul D. Taylor c, J. William Schopf d,e,f,g,h, Anatoliy B. Kudryavtsev e,g,h, Julie Bailey-Brock i a The Australian Museum, 6 College Street, Sydney, NSW 2010, Australia b Department of Geology, University of Tartu, Ravila 14A, 50411 Tartu, Estonia c Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK d Department of Earth, Planetary, and Space Sciences, USA e Center for the Study of Evolution and the Origin of Life, USA f Molecular Biology Institute, University of California, Los Angeles, CA 90095, USA g PennState Astrobiology Research Center, University Park, PA 16802, USA h University of Wisconsin Astrobiology Research Consortium, Madison, WI 53706, USA i Biology Department of Zoology, University of Hawaii at Manoa, 2538 McCarthy Mall, Honolulu, HI 96822, USA article info abstract Article history: Although the carbonate compensation depth (CCD) for calcite, generally located in the depth range Received 17 December 2013 4000–5000 m, is often proposed as a physiological barrier to deep-ocean colonization, many organisms Received in revised form with calcareous exoskeletons are found in the deepest oceanic trenches. Serpulid polychaetes inhabiting 11 April 2014 unprotected calcareous tubes are unlikely deep-sea inhabitants, yet, they are found at all oceanic depths Accepted 15 April 2014 from intertidal to hadal. Here we review and revise the published and unpublished records of Serpulidae Available online 24 April 2014 from below 5000 m depth. We also describe tube ultrastructure and mineralogical content of available Keywords: deep-sea serpulid tubes to obtain insights into their biomineralisation. Species belonging to the genera Polychaeta Bathyditrupa, Bathyvermilia, Hyalopomatus, Pileolaria (spirorbin) and Protis were found at depths from Serpulidae 5020 to 9735 m. However, only specimens of Protis sp. were truly hadal (46000 m) being found at Abyssal 6200–9700 m. Hadal specimens of Protis have irregularly oriented prismatic tube microstructure similar Hadal Carbonate compensation depth to that found in more shallow-water representatives of the genus. Initial EDX analysis suggested a mostly Tube ultrastructure calcitic composition (i.e., the most stable CaCO3 polymorph) on the basis of high Mg levels. Surprisingly, Mineral composition however, tubes of Bathyditrupa hovei and a species of Protis analysed using the more reliable method of laser Raman spectroscopy were found to be composed of aragonite. The compensation depth for this less stable CaCO3 polymorph in the oceans is usually 2000–3000 m. We found no obvious structural adaptations to life at extreme depths in the studied serpulid tubes and how serpulids are able to biomineralise and maintain their tubes below the CCD remains to be explained. Crown Copyright & 2014 Published by Elsevier Ltd. All rights reserved. 1. Introduction (e.g., holothurians, and soft and organic-walled foraminifera, see Nozawa et al. (2006)). At 4000–5000 m there is the “Carbonate Calcium carbonate is widely used as a structural skeletal Compensation Depth” (CCD) at which calcium carbonate (calcite component by marine invertebrates, such as crustaceans, echino- and aragonite) supply equals the rate of dissolution (e.g., Bickert, derms, foraminiferans, corals and molluscs (e.g., Cuif et al., 2011). 2009). However, although the CCD has been commonly proposed Because carbonate solubility increases with increasing pressure, as a physiological barrier to deep-ocean colonization (e.g., biomineralisation becomes more difficult with increasing depth Blankenship-Williams and Levin, 2009), some bryozoans and and this has been proposed as an explanation (Jamieson et al., molluscs are found below these depths (e.g., Hayward, 1984: 2010) of why some groups with calcareous skeletons (e.g., ophiur- cheilostome bryozoans; Knudsen, 1970: bivalves; Leal and oids and echinoids) tend to be replaced by soft-bodied organisms Harasewych, 1999: cocculinid and pseudococculinid limpets). How species with external calcareous skeletons persist below the CCD remains one of the most intriguing questions of modern ☆Author contributions: EKK wrote most of the first draft of the manuscript, parts deep-sea biology. One obvious explanation is that these calcareous on biomineralisation were also written by OV and PDT, EKK and JBB are responsible exoskeletons do not come into direct contact with seawater, but for diagnoses and illustrations of deep-sea species, OV and PDT did SEM and EDX are protected by thick organic layers, the structure and composi- mineralogical analyses, JWS and AK did Raman mineralogical analyses. n Corresponding author. tion of which vary widely amongst organisms. The calcareous E-mail address: [email protected] (E.K. Kupriyanova). exoskeletons of molluscs typically are externally covered with an http://dx.doi.org/10.1016/j.dsr.2014.04.006 0967-0637/Crown Copyright & 2014 Published by Elsevier Ltd. All rights reserved. 92 E.K. Kupriyanova et al. / Deep-Sea Research I 90 (2014) 91–104 organic layer (periostracum) that could protect against carbonate Natural History Museum, London (NHMUK). Back-scattered elec- dissolution (Harper, 1997; Taylor and Kennedy, 1969), and crusta- trons were used to form images of these uncoated tubes. cean carapaces are covered with a thick epicuticle. Molluscs largely exposed to ambient seawater, such as scallops and oysters, 2.3. Mineralogical composition are not found in the lower abyssal zone. For example, the deep-sea oyster Neopycnodonte zibrowii (Gofas et al., 2009) occurs in a The elemental compositions of the deep-sea serpulid tubes were bathymetric range between 350 and 846 m (Van Rooij et al., 2010). determined using an Oxford Instruments X-max EDX detector Serpulid polychaetes inhabiting calcareous tubes that lack any attached to the LEO 1455-VP SEM at the NHMUK. The main objective external protective layers are the most unlikely inhabitants of the was to infer tube mineralogy using Mg and Sr as proxies for calcite deepest parts of the ocean. However, these sedentary suspension and aragonite, respectively. However, because the tubes were not feeders are found from intertidal to abyssal and even hadal depths flat, polished surfaces, these proxies proved to be unreliable. (e.g., Bruun, 1957; ten Hove and Kupriyanova, 2009; Kupriyanova Laser Raman spectroscopy was undertaken at the University of et al., 2011; Levenstein, 1973; Zibrowius, 1977). Vinn and California, Los Angeles (UCLA). Spectroscopic data were obtained Kupriyanova (2011) hypothesised that dense outer layers (DOL) using a T64000 triple-stage laser Raman system (JY Horiba, Edison, giving a smooth shiny appearance to the tube surface evolved as NJ, USA) with macro-Raman and confocal micro-Raman capabil- an adaptation to delay tube dissolution in waters of the deep-sea ities. A Coherent Innova 90 argon ion laser (Santa Clara, CA, USA) under-saturated with respect to calcium carbonate, but this idea provided several laser wavelengths in the blue-green region of the based on a very limited sample size still requires testing. visible spectrum. A single spectral window centred at 1400 cm–1 The deepest parts of the oceans (6000–11,000 m), known as the was employed. For the laser excitation used, at 488 nm, this gave ultra-abyssal (Belyaev, 1989) or hadal zone, are represented almost coverage from 140 to 2650 cm–1, a range containing all of the exclusively by trenches. To date, published records of serpulids major Raman bands of calcite and aragonite. For analysis, speci- from depths below 6000 m are very scarce. Zibrowius (1977), who mens were centred in the path of the laser beam projected reviewed serpulids from depths exceeding 2000 m, listed 25 through an Olympus BX41 microscope (Olympus, Center Valley, species, including only one unidentifiable specimen from the PA, USA). Typical laser power was 1–8 mW over a 1 mm spot, an Kermadec Trench collected at 6620–6730 m (Kirkegaard, 1956). instrumental configuration well below the threshold causing In his influential book on hadal faunas, Belyaev (1989), in addition radiation damage to specimens of the kind studied here. Point to the record of Kirkegaard (1956), listed two unidentified Serpu- spectra were obtained from various parts of the interior and lidae from 6410 to 6757 m (Aleutian Trench) and 9715–9735 m exterior surfaces of the serpulid tubes. (Izu-Bonin Trench), the latter being the deepest record for a serpulid. More recently, Kupriyanova et al. (2011) reviewed all previous reports of abyssal serpulids and provided new records 3. Results based on collections by the R/V “Vityaz”, including Bathyditrupa hovei Kupriyanova, 1993 from 6050 to 6330 m. 3.1. Taxonomy The aims of the current study are to review and revise published and unpublished records of serpulids collected below the CCD The serpulid species found below 5000 m are summarized in (5000 m and deeper), and to address the question whether the tube Table 1. A short taxonomic account of these records with informa- ultrastructure and mineralogy of these calcareous tube-building tion on their tube ultrastructure is given below. polychaetes show functional adaptations to deep-sea habitats. Genus Bathyditrupa Kupriyanova, 1993a 2. Material and methods Remarks. This monotypic genus appears to be closely related