Original PaperEyes of the Deep-sea Floor: The Integrative Taxonomy of the Foraminiferal Genus Vanhoeffenella
Introduction
The deep seafloor harbors an immense diversity of foraminifera, spanning the size range from less than 50 microns to several centimeters in the case of the giant xenophyophores. Monothalamous (single-chambered) foraminifera (‘monothalamids’; Pawlowski et al. 2013) are particularly abundant in the deep sea as well as at high-latitudes, but are also present in coastal and freshwater habitats (Gooday et al., 2004, Habura et al., 2008, Holzmann et al., 2003, Nozawa et al., 2006, Voltski and Pawlowski, 2015). Monothalamids are either naked (cells devoid of tests) or testate protists in which the test is composed of organic or agglutinated material. In the latter case the organic component serves as the basal layer or binding agent for agglutinated particles, with some species constructing complex composite tests consisting of two or three distinct components that may differ quite radically in their morphology and construction. Traditional classifications divided monothalamous foraminifera into organic-walled allogromids and agglutinated astrorhizids (Loeblich and Tappan, 1987, Sen Gupta, 2002). Molecular phylogenies have challenged this simple morphology-based system by showing that the organic-walled and agglutinated species branch together, prompting the division of monothalamids into a number of clades that often lack a clear morphological identity (Pawlowski et al., 2002, Pawlowski et al., 2011).
Vanhoeffenella is a cosmopolitan genus of deep-sea monothalamids (Gooday and Jorissen 2012). It was first described by Rhumbler (1905) from the Southern Ocean with the type species Vanhoeffenella gaussi, named after the famous German research vessel Gauss which, in 1901–1903, explored the unknown region of the Southern Ocean, south of the Kerguelen Islands. These foraminifera sometimes have a distinctive eye-like appearance, owing to their unusual, partially transparent secondary test. Despite its ubiquitous distribution in the deep sea, practically nothing is known about the diversity within Vanhoeffenella. The type species has been reported from various locations around the world, predominantly from deep-sea settings (Cornelius and Gooday, 2004, Earland, 1933, Gooday et al., 2004, Heron-Allen and Earland, 1922, Hofker, 1972, Hughes et al., 2000, Shchedrina, 1979, Wollenburg, 1992, Wollenburg, 1995), but also from shelf depths (Christiansen, 1958, Majewski et al., 2007, Majewski and Anderson, 2009). However, many of these records are based on specimens that differ morphologically from each other and from the original type species. This has led to the suggestion that many species inhabit the World Ocean (Gooday et al. 2004). Unfortunately, Vanhoeffenella has received little attention among foraminiferal taxonomists. Apart from V. gaussi, only three species have been briefly described, one of them from the Southern Ocean (V. oculus Earland 1933), one from subantarctic waters near Kerguelen islands (V. foliacea Shchedrina 1979), and one from the Arctic (V. cardioformis Shchedrina 1979). In addition, molecular data have not fully clarified the phylogentic position of Vanhoeffenella (Pawlowski et al. 2002). A few previously analysed specimens (Pawlowski et al. 2002) have yielded ambiguous results. Some sequences were attributed to Clade F and others to the enigmatic Clade V, one of the most widespread monothalamid groups in the deep sea (Lecroq et al., 2011, Pawlowski et al., 2011).
The present paper is based on morphological and molecular data obtained from an extensive collection of Vanhoeffenella specimens obtained from the Atlantic, Southern and Arctic Oceans. Our aims are to 1) describe the diversity of Vanhoeffenella based on a combination of morphological and genetic data, 2) provide new information about the commonly reported type species (V. gaussi) and the poorly known V. oculus, and 3) establish a new species, V. dilatata.
Section snippets
Isolates, Sequences and Molecular Phylogeny
The targeted gene fragment was successfully amplified for 33 of the 69 specimens processed for DNA extraction (Table 1). 22 specimens gave good quality sequences, all branching within Clade F of monothalamous foraminifera. 4 sequences obtained earlier (ForamDNA #8212 [2 clones] from Admiralty Bay, and ForamDNA #3291 and 3256 from the Weddell Sea) were also used. These 26 sequences were deposited in GenBank under accession numbers MF457668 - MF457735. The sequencing of one individual (ForamDNA
Arctic (‘ARK’) Vanhoeffenellids
The earliest record of Vanhoeffenella from the Arctic belongs to Shchedrina (1979), who described a single species (V. cardioformis) from the Laptev Sea. It had a narrow agglutinated rim and unlike any of the specimens that we found in the Arctic Ocean it had 3 arms. However, it is unclear whether the number of arms is an important morphological criterion by itself, as in V. gaussi the number increases with the test size. Too few Arctic Vanhoeffenella isolates have been found to draw any
Methods
Sampling: Vanhoeffenella individuals were collected during research cruises in the Atlantic, Southern and Arctic Oceans over a period of eleven years (2002–2013). In the Atlantic, most of the material came from the northern and south-western parts of the Ocean (projects IceAGE2, R/V Poseidon, and BIOSKAG II, R/V Håkon Mosby), with the exception of a few samples obtained during the DIVA 3 expedition (R/V Meteor) in the central western Atlantic. The Southern Ocean samples were collected mainly in
Acknowledgements
We thank three reviewers for their insightful comments and corrections of the earlier version of this paper. We are also grateful to Angelika Brandt, Klaus Hausmann and Pedro Martinez for their invitations to participate in research cruises; Cyril Obadia, Delia Fontaine, Franck Lejzerowicz, Tomas Cedhagen, Sarah Schnurr and Wojciech Majewski who helped to collect the material, and to Klaus Hausmann and Alexander Kudryavtsev for some micrographs taken during DIVA 3 cruise.
The study was supported
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