Agglutinated foraminifera are marine protists that show apparently complex
behaviour in constructing their shells, involving selecting suitable
sedimentary grains from their environment, manipulating them in three
dimensions, and cementing them precisely into position. Here we illustrate a
striking and previously undescribed example of complex organisation in
fragments of a tube-like foraminifer (questionably assigned to
Agglutinated foraminifera are unicellular organisms that construct their shells from sedimentary grains gathered from the sea-floor environment and cement them together to form what are sometimes intricate three-dimensional constructions (Brady, 1879; Gooday, 1990). To do this they must select, orientate and secure the grains in ways that are, at present, poorly understood (Allen et al., 1988; Hemleben and Kaminski, 1990; Makled and Langer, 2010; Rothe et al., 2011). The use of grain type can seem relatively haphazard (Armynot du Châtelet et al., 2013) or it can be highly selective of both size and composition. Examples of selectivity include foraminifera that gather specific minerals, sometimes heavy ones, such as ilmenite (Makled and Langer, 2010), rutile (Cole and Valentine, 2006) and garnet (Allen et al., 1999), or particular biological clast types such as sponge spicules (Brady, 1879), echinoderm plates (Heron-Allen and Earland, 1909), or coccoliths (Holbourn and Kaminski, 1997; Thomsen and Rasmussen, 2008). It is also common for some agglutinated foraminifera to re-use the shells of dead planktonic foraminifera from the surrounding sediment in constructing their tubes (Brady, 1879; Cartwright et al., 1989).
Tube-like agglutinated foraminifera that use planktonic foraminifer shells in
their construction are common in bathyal and abyssal environments worldwide,
where they live either as suspension or deposit feeders (Gooday, 1990).
Fragments are difficult to assign to genus level if the proloculus is absent
and the branching pattern unclear, as is the case with the pieces described
here. The most important genera that secrete such tubes are
A fragment of
Here we illustrate four fragments of what was probably a single tube, which are remarkable because the individual grains belong to a single species of planktonic foraminifer and occur in an organised arrangement. We also show one specimen of
Particles from the sediment in IODP Sample U1482B-mudline.
The
Four SEM images of the tube successively rotated forward by
approximately 70
The four fragments of ?
A total of 123 planktonic foraminifer shells are cemented along the tube of
the largest fragment, all of which belong to the single species,
The construction of the matrix also implies considerable selectivity because detrital grains are a relatively minor component of the very fine fraction sediments recovered at this location, compared to biogenic grains such as coccoliths, which are entirely excluded (although they can be seen adhering to the specimen in places, which was only gently cleaned). The binding cement appears to be very strong because planktonic foraminifer shells at both broken ends of the tube are fractured through the middle rather than having been detached at their edges (see Fig. 2c, e).
The most notable feature of the specimen is the regular way in which
Although to our knowledge
The
The phenomenon seems to belong to a different category from cases in which
unicellular organisms such as other foraminifera, radiolaria, and diatoms
secrete intricate skeletons of silica or carbonate as part of their life
cycle (see, for instance, Fig. 3). In those cases the biomineralisation
sequence is presumably under genetic and epigenetic control in which
information is stored in genes which switch on or off in response to internal
triggers. In the case of complex agglutinating behaviour, the correct grain
type must be discovered by the pseudopodial network, transported to the
precise location required, and then manipulated in three dimensions before
being cemented into place. At some point in the process it must be
discriminated from other similar grains. We suggest two possible models for
how this discrimination occurs. Either (1) it occurs via a highly specific
trial-and-error process at the site of cementation to which many grains are
brought and rejected, and only
Much behaviour in protists is apparently highly stereotyped and involves chemosensory responses to environmental cues in relation to feeding, predator avoidance, and discriminating clones and potential mates (Vandromme et al., 2010; Harvey et al., 2013). However recent work on partner recognition in some ciliates has concluded that they are able to actively encode, process and respond to information from external pheromone signals which in turn produces planned “courtship strategies” and “social decision making” (Clark, 2013). In the agglutinated foraminifer cell discussed here, the decision-making must also, presumably, have a specialised molecular basis, whether it occurs at the site of cementation or distributed in the pseudopodial network. As far as we know, such processes are obscure, but if they can occur in one type of cell, they could occur in others, so the phenomenon could be more than just a curiosity.
Seawater and sediment slurry from the top of the first piston core at IODP
Hole U1482B was collected in a bucket, treated with rose bengal biological
stain for 24 h to detect living cells and washed over 150 and
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The data to this paper can be found in the Supplement.
The supplement related to this article is available online at:
Ivano W. Aiello (Geological Oceanography, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA 95039-9647, USA), Tali L. Babila (Ocean Sciences Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, USA), Germain Bayon (Unité Géosciences Marines, Institut Francaise de Recherche pour l'Exploitation de la Mer (IFREMER), 29280 Plouzané, France), Luc Beaufort (Centre Europén de Recherche et d'Enseignement de Géologie de l'Environnement (CEREGE) BP80, Centre National de la Recherche Scientifique (CNRS), Aix-Marseille Université, Ave L. Philbert, 13545 Aix-en-Provence, France), Samantha C. Bova (Institute of Marine and Coastal Sciences, Rutgers, The State University of New Jersey, 71 Dudley Road, New Brunswick, NJ 08901-8521, USA), Jong-Hwa Chun (Petroleum and Marine Research Division, Korea Institute of Geoscience and Mineral Resources (KIGAM), 124 Gwahnag-no, Yuseong-gu, Daejeon 305-350, Korea), Haowen Dang (State Key Laboratory of Marine Geology, Tongji University, 1239 Siping Road, Shanghai 200092, P.R. China), Anna Joy Drury (MARUM, University of Bremen, Leobener Str., 28359 Bremen, Germany), Tom Dunkley Jones (School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK), Patrícia P. B. Eichler (Department of Geophysics, Geodynamics and Geology, Federal University of Rio Grande do Norte, Campus Universitário, Lagoa Nova, Natal RN 59078-970, Brazil), Fernando Allan Gil Salazar (National Institute of Geological Sciences, University of the Philippines, Diliman, Quezon City 1101, Philippines), Kelly Gibson (SEOE, University of South Carolina, 701 Sumter Street, EWS 617, Columbia, SC 29208, USA), Robert G. Hatfield (College of Earth, Ocean and Atmospheric Sciences, Oregon State University, 104 CEOAS Admin. Building, Corvallis, OR 97331, USA), Ann E. Holbourn (Institute of Geosciences, Christian-Albrechts-Universität zu Kiel, Ludewig-Meynstr. 10–14, 24118 Kiel, Schleswig Holstein, Germany), Daniel L. Johnson (Department of Geological and Planetary Sciences, California Institute of Technology, 1200 E. California Boulevard, Pasadena, CA 91125, USA), Denise K. Kulhanek (International Ocean Discovery Program, Texas A&M University, 1000 Discovery Drive, College Station, TX 77845, USA), Yuho Kumagai (Department of Earth Science, Tohoku University, Aoba 6-3, Sendai 980-8578, Japan), Tiegang Li (The First Institute of Oceanography, SOA, 7 Nanhai Road, 6 Xian Xialing Rd. 266061, P.R. China), Braddock K. Linsley (Lamont-Doherty Earth Observatory, Columbia University Geoscience 104, 61 Route 9W, Palisades, NY 10964, USA), Niklas Meinicke (Department of Earth Science, University of Bergen, Norway, Allegaten 41, 5007 Bergen, Norway), Gregory S. Mountain (Department of Earth and Planetary Sciences, Rutgers, The State University of New Jersey, 610 Taylor Road, Piscataway, NJ 08854-8066, USA), Bradley N. Opdyke (Research School of Earth Sciences, Australian National University, Canberra ACT 0200, Australia), Christopher R. Poole (Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK), Christina Ravelo (Ocean Sciences Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, USA), Yair Rosenthal (Institute of Marine and Coastal Sciences, Rutgers, The State University of New Jersey, 71 Dudley Road, New Brunswick, NJ 08901-8521, USA), Takuya Sagawa (Institute of Science and Engineering, Kanazawa University, Kakuma-machi, Kanazawa 920-1192, Japan), Anaïs Schmitt (Faculty of Science and Technology, Université de Nantes, 2 rue de la Houssinière, 44322 Nantes, France), Jennifer B. Wurtzel (Research School of Earth Sciences, Australian National University, Canberra ACT 0200, Australia), Jian Xu (Department of Geology, Northwest University, 229 North Taibai Road, Xi'an Shaanxi 710069, P.R. China), Masanobu Yamamoto (Faculty of Environmental Earth Science, Hokkaido University, Kita-10, Nishi-5, Kita-ku, Sapporo 060-0810, Japan), and Yi Ge Zhang (Texas A&M University, Department of Oceanography, MS 3146, College Station, TX 77843, USA).
The authors declare that they have no conflict of interest.
We thank Bill Crawford for ship-board photography, Wolfgang Kuhnt for advice, and Trevor Dale for stimulating discussion. Edited by: Laia Alegret Reviewed by: Andrew Gooday and one anonymous referee