As Earth's high-CO2 atmosphere drives changes in ocean chemistry, marine carbonate geochemists are delving into the composition of marine skeletons, with a view to understanding possible effects on dissolution and calcification. Detailed studies of skeletal carbonate mineralogy have revealed more complexity and variability than originally assumed. Some coralline algae, for example, far from being entirely high-magnesium calcite as had long been thought, have been shown to contain low-Mg calcite and even aragonite (Smith et al., 2012). Similarly, invertebrates such as bryozoans (Smith, Key & Gordon, 2006; Taylor et al., 2009) and serpulid worms (Smith, Riedi & Winter, 2013) have proved to be mineralogically complex, with variability related to phylogeny, environment and/or skeletal element. Smaller skeletal elements, such as radulae or statoblasts of varying compositions, can add to the biomineral complexity. Molluscs in particular are known to exert a great deal of control over many various minerals they precipitate; some cephalopod species may secrete more than 10 different minerals (Smith, 2012).

Scaphopods appear to be a group awaiting mineralogical study. Of the 10 or so shells actually tested (Clarke & Wheeler, 1917, 1922; Bøggild, 1930; Alzuria, 1984), all are from the North Atlantic or Mediterranean and all belong to the family Dentaliidae (Table 1). They encompass seven species (there is almost no replication) and all 10 shell specimens have been shown to be aragonitic, low in magnesium and strontium. The radular teeth in (at least some) scaphopods may be mineralized, perhaps with an amorphous calcium phosphate with, sometimes, iron and copper in the teeth (Vovelle & Grasset, 1983; but see Glover, Taylor & Whittaker, 2003). There may be gravity receptors (statocysts), larval stages or protoconchs which could be mineralized, but nothing is known about the mineralogy of these life stages. It is quite an extrapolation to assert that all 500 or so species of scaphopods from around the world are always aragonitic (e.g. de Paula & Silveira, 2009) on the basis of such a small set of measurements (10 specimens, seven species, all in a single family). We set out to determine whether there is more mineralogical variability among scaphopods by studying material from a wide range of families and geographic areas.

Table 1.

Published and new data on the skeletal mineralogy of scaphopods.

Order Family Species Specimens Mean wt% Calcite Mean wt% MgCO3 Mineralogy Reference 
Dentaliida Dentaliidae Antalis agilis (G.O. Sars, 1872) Aragonite This study 
Antalis bouei (Deshayes, 1825) Aragonite Bøggild (1930
Antalis dentalis (Linnaeus, 1758) 2 radulae   ACP, Fe, Cu found Vovelle & Grasset (1983) 
Antalis entalis (Linnaeus, 1758) Aragonite Bøggild, 1930 
Antalis entalis (Linnaeus, 1758) Aragonite This study 
Antalis inaequicostata (Dautzenberg, 1891) Aragonite Alzuria (1984
Antalis nana (Hutton, 1873) 45 Aragonite This study 
Dentalium decussatum  J. Sowerby, 1814 Aragonite Bøggild (1930
Dentalium panormum Chenu Aragonite This study 
Dentalium octangulatum Donovan, 1804 Aragonite This study 
Dentalium rugiferum von Koenen, 1885 Aragonite Bøggild (1930
Fissidentalium candidum (Jeffreys, 1877) 0.2 Aragonite Clarke & Wheeler (1917, 1922
Fissidentalium exuberans (Locard, 1891) Aragonite This study 
Fissidentalium shoplandi (Jousseaume, 1894) 13 Aragonite This study 
Fissidentalium zelandicum (Sowerby, 1860) 38 Aragonite This study 
Fissidentalium zelandicum (Sowerby, 1860) 3 radulae   no minerals present This study 
Gadilida Entalinidae Bathoxiphus ensiculus (Jeffreys, 1877) Aragonite This study 
Entalina tetragona (Brocchi, 1814) 0.3 1.1 Aragonite (tr LMC) This study 
Gadilidae Cadulus cylindratus (Jeffreys, 1877) Aragonite This study 
Cadulus euloides (Melvill & Standen, 1901) 0.3 Aragonite (tr LMC) This study 
Polyschides cf. tetraschistus (Watson, 1879) Aragonite This study 
Siphonodentalium lobatum (Sowerby, 1860) Aragonite This study 
Order Family Species Specimens Mean wt% Calcite Mean wt% MgCO3 Mineralogy Reference 
Dentaliida Dentaliidae Antalis agilis (G.O. Sars, 1872) Aragonite This study 
Antalis bouei (Deshayes, 1825) Aragonite Bøggild (1930
Antalis dentalis (Linnaeus, 1758) 2 radulae   ACP, Fe, Cu found Vovelle & Grasset (1983) 
Antalis entalis (Linnaeus, 1758) Aragonite Bøggild, 1930 
Antalis entalis (Linnaeus, 1758) Aragonite This study 
Antalis inaequicostata (Dautzenberg, 1891) Aragonite Alzuria (1984
Antalis nana (Hutton, 1873) 45 Aragonite This study 
Dentalium decussatum  J. Sowerby, 1814 Aragonite Bøggild (1930
Dentalium panormum Chenu Aragonite This study 
Dentalium octangulatum Donovan, 1804 Aragonite This study 
Dentalium rugiferum von Koenen, 1885 Aragonite Bøggild (1930
Fissidentalium candidum (Jeffreys, 1877) 0.2 Aragonite Clarke & Wheeler (1917, 1922
Fissidentalium exuberans (Locard, 1891) Aragonite This study 
Fissidentalium shoplandi (Jousseaume, 1894) 13 Aragonite This study 
Fissidentalium zelandicum (Sowerby, 1860) 38 Aragonite This study 
Fissidentalium zelandicum (Sowerby, 1860) 3 radulae   no minerals present This study 
Gadilida Entalinidae Bathoxiphus ensiculus (Jeffreys, 1877) Aragonite This study 
Entalina tetragona (Brocchi, 1814) 0.3 1.1 Aragonite (tr LMC) This study 
Gadilidae Cadulus cylindratus (Jeffreys, 1877) Aragonite This study 
Cadulus euloides (Melvill & Standen, 1901) 0.3 Aragonite (tr LMC) This study 
Polyschides cf. tetraschistus (Watson, 1879) Aragonite This study 
Siphonodentalium lobatum (Sowerby, 1860) Aragonite This study 

Details of collection and locations are available on request. Species names after Steiner & Kabat (2004).

It is, perhaps, not surprising that very little is known about the skeletal carbonate mineralogy of the Scaphopoda. They are relatively rare and often buried in soft sediments from intertidal waters (Glover et al., 2003) down to abyssal depths (4500 m) (Mulcrone, 2005). The shell is a long, narrow, slightly curved cone (hence ‘tusk shells'), open at both ends. Scaphopod shells are usually 2 to 4 cm long, but can range from about 0.5 to 15 cm; some fossils are reportedly up to 30 cm long (Mulcrone, 2005). The scaphopod fossil record stretches back to at least the Carboniferous and possibly the Ordovician (about 460 Ma). They were probably the last molluscan class to evolve, although their relationships to other classes remain unclear (Schrödl & Stöger, 2014).

There are two recognized orders in the class Scaphopoda. The Dentaliida are characterized by having the widest part of the shell at the aperture, with the outer surface often longitudinally sculptured and the middle radular tooth broader than it is high (Habe, 1964; Reynolds & Okusu, 1999). There are eight families in the order and about 290 species, the vast majority in the family Dentaliidae (Steiner & Kabat, 2001, 2004). In contrast, in the Gadilida the widest part of the shell is somewhat behind the aperture. They are usually completely smooth on the outside and the middle radular tooth is higher than it is wide (Habe, 1964; Reynolds & Okusu 1999). This order contains four families with about 560 species (Steiner & Kabat, 2001, 2004).

Very little is known about biomineralization in scaphopods. In their comprehensive review of biomineralization, Lowenstam & Wiener (1989: 94) stated only this: “The shell is composed of aragonite (Bøggild, 1930) and is differentiated into three layers: a thick middle layer (crossed-lamellar ultrastructure) and two thin surface layers (homogeneous or finely prismatic) (Bøggild, 1930). The mantle is completely fused into a cylindrical cone. Almost nothing appears to be known about the shell formation processes of Scaphopoda.”

A detailed search of the literature has found little more. A few studies have investigated scaphopod shell structure (Couvreur, 1979; Alzuria, 1984), protoconchs (Engeser, Riedel & Bandel, 1993) and the composition of radulae (Vovelle & Grasset, 1983; Glover et al., 2003). Most studies cite only Bøggild (1930), who published results on four species, for the mineralogy of this class.

In order to address this shortfall in data, we acquired scaphopod shells from around the world from collections at: Natural History Museum (NHM), National Institute of Water and Atmosphere (New Zealand), National Museum of Scotland (NMS), Auckland Museum (AM) and Museum of New Zealand Te Papa Tongarewa (MNZ), focusing in particular on families whose mineralogy has heretofore been unknown. In addition, we have collected scaphopods from around New Zealand, with the animal intact. Here we report on the shell mineralogy of 21 species of scaphopods, including replication within shells and among individuals from the same population (number of replicate specimens ranged from 1 to 45, average 8.6). The distribution of sampled individuals ranged from the South Pacific to the North Atlantic. One specimen of Antalis nana was coated with Au/Pd and examined under SEM for mineral ultrastructure. For three specimens of Fissidentalium zelandicum, we dissected out the radulae and examined them for mineral composition under Raman spectroscopy (Nehrke & Nouet, 2011).

Dead tissue and/or encrusting material was removed from each shell mechanically and a brief period (30 min or less) of bleaching (5% household bleach) assisted in removing organic material. Large specimens were sectioned along the length of the shell into 3 to 10 samples, whereas small specimens formed one sample each. Samples were powdered to crystallites, spiked with 0.1 g halite (NaCl) as an internal standard and smeared onto a glass slide for X-ray diffractometry (XRD) analysis (following the calibration and methods of Gray & Smith, 2004).

A total of 135 specimens from 14 species in three families were analysed for mineralogy to add to the published literature, providing a total of 146 specimens in 21 species (Table 1). Shells of individuals from all species proved to be composed of 100% aragonite, although most specimens of the entalinid Entalina tetragona and all specimens of the gadilid Cadulus euloides showed traces (0.2–0.4 wt% calcite) of low-magnesium (0 to 2.3 wt% MgCO3) calcite; that level is at the limit of the precision of the technique, but was consistently noted among just those specimens. All within-individual measurements on Fissidentalium zelandicum were 100% aragonite. SEM micrographs of an Antalis nana shell (collected alive) showed a heavily bored outer surface, with cross-lamellar aragonitic tablets, sometimes connected by microtubules (Fig. 1).

Figure 1.

Shell microstructure of Antalis nana, collected alive off Stewart Island, New Zealand. A, B. Heavily bored outer layer. C, D. Stacked aragonite tablets with small tubules joining them (D). E. Cross-section of shell, showing cross-lamellar arrangement of tablets. F. Detail of cross-lamellar layers. Scale bars: A, B, E = 10 µm; C, F = 1 µm; D = 100 nm.

Figure 1.

Shell microstructure of Antalis nana, collected alive off Stewart Island, New Zealand. A, B. Heavily bored outer layer. C, D. Stacked aragonite tablets with small tubules joining them (D). E. Cross-section of shell, showing cross-lamellar arrangement of tablets. F. Detail of cross-lamellar layers. Scale bars: A, B, E = 10 µm; C, F = 1 µm; D = 100 nm.

We were unable to detect any mineralized material in the Fissidentalium zelandicum radulae that were examined. It appears they are predominantly chitinous (like most gastropods but conspicuously unlike chitons or limpets, e.g. Brooker & Shaw, 2012).

We now know the skeletal carbonate mineralogy of 21 species from both hemispheres and 3 of the 12 families in the class; a total of 4% of known species have now been measured (Table 2). It appears that the generalizations of early authors were right. All scaphopods so far studied produce entirely aragonitic skeletons, though some of the gadilidan scaphopods were found to contain small amounts of very low-Mg calcite, comprising no more than 1% of the skeletal weight, and thus below the precision level of the technique used. Such very small tubes are difficult to clean completely and a tiny grain or infilled boring (e.g. a foraminiferan) could have produced contamination.

Table 2.

Known and unknown mineralogy of families in the class Scaphopoda (taxonomy follows Steiner & Kabat, 2004).

Order Family Generaa Extant species Species for which mineralogy is known Percentage known Shell mineralogy 
Dentaliida Anulidentaliidae Anulidentalium, Epirhabdoides 0%  
Calliodentaliidae Calliodentalium 0%  
Dentaliidae Antalis, Coccodentalium, Compressidentalium, Dentalium, Dudentalium, Fissidentalium, Graptacme, Paradentalium, Pictodentalium, Plagioglypta, Schizodentalium, Striodentalium, Tesseracme 227 14 6% Aragonite 
Fustiariidae Fustiara 15 0%  
Gadilinidae Episiphon, Gadilina 25 0%  
Laevidentaliidae Laevidentalium 14 0%  
Omniglyptidae Omniglypta 0%  
Rhabdidae Rhabdus 0%  
Gadilida Entalinidae Bathoxiphus, Costentalina, Entalina, Entalinopsis, Heteroschismoides, Pertusiconcha, Rhomboxiphus, Solenoxiphus, Spadentalina 33 6% Aragonite 
Gadilidae Bathycadulus, Cadulus, Dischides, Gadila, Polyschides, Sagamicadulus, Siphonodentalium, Striocadulus 205 2% Aragonite 
Pulsellidae Annulipulsellum, Pulsellum, Striopulsellum 25 0%  
Wemersoniellidae Chistikovia, Wemersoniella 0%  
Order Family Generaa Extant species Species for which mineralogy is known Percentage known Shell mineralogy 
Dentaliida Anulidentaliidae Anulidentalium, Epirhabdoides 0%  
Calliodentaliidae Calliodentalium 0%  
Dentaliidae Antalis, Coccodentalium, Compressidentalium, Dentalium, Dudentalium, Fissidentalium, Graptacme, Paradentalium, Pictodentalium, Plagioglypta, Schizodentalium, Striodentalium, Tesseracme 227 14 6% Aragonite 
Fustiariidae Fustiara 15 0%  
Gadilinidae Episiphon, Gadilina 25 0%  
Laevidentaliidae Laevidentalium 14 0%  
Omniglyptidae Omniglypta 0%  
Rhabdidae Rhabdus 0%  
Gadilida Entalinidae Bathoxiphus, Costentalina, Entalina, Entalinopsis, Heteroschismoides, Pertusiconcha, Rhomboxiphus, Solenoxiphus, Spadentalina 33 6% Aragonite 
Gadilidae Bathycadulus, Cadulus, Dischides, Gadila, Polyschides, Sagamicadulus, Siphonodentalium, Striocadulus 205 2% Aragonite 
Pulsellidae Annulipulsellum, Pulsellum, Striopulsellum 25 0%  
Wemersoniellidae Chistikovia, Wemersoniella 0%  

aGenera in bold have had at least one sample tested for mineralogy.

We found no significant variation in skeletal mineralogy within individual skeletons, among individuals or among families. This result is uncharacteristic of molluscs—chitons, bivalves, gastropods and especially cephalopods are well known to use diverse minerals, some of which are not found elsewhere among biomineralizing taxa, and to exert both control and finesse to produce complex multilayered skeletons, often with a strong phylogenetic overprint (e.g. Bøggild, 1930). Nevertheless, the class Scaphopoda is extremely conservative morphologically, and the uniformity in mineralogy may simply be a reflection of this wider homogeneity.

Aragonite, as the metastable and more soluble polymorph of CaCO3, is considered to be more susceptible to dissolution than its calcite counterpart (e.g. Andersson, Mackenzie & Bates, 2008). Under the future-ocean scenario of warming and acidification, aragonitic shells may be at greater risk. Scaphopods, however, may be insulated from ocean acidification by the water depths they inhabit. Many of the specimens studied here were collected at water depths greater than 100 m; these scaphopods may not be affected by surface-driven global climate change for a considerable time. On the other hand, if the aragonite saturation horizon shoals rapidly in the Southern Ocean, as some studies suggest (Feely et al., 2012), deep-dwelling aragonitic scaphopods might well be at risk.

ACKNOWLEDGEMENTS

Many thanks to Mary Spencer Jones and Kathie Way at NHM, Sankurie Pye at NMS, Wilma Blom at AM and Bruce Marshall at MNZ, for the kind loan of scaphopod material from their collections. Bill Dickson and Phil Heseltine were, as always, stalwart assistants on the RV Polaris II cruises. Thanks to Chris Garden, Marc Riedi, Bruce Hayward and Margaret Morley for assistance in the field, to Christine Davis and Johanna Brinkman for XRD work, to Liz Girvan at the Otago Centre for Electron Microscopy for SEM support, to Ken Miller for assistance with the figure and to Bryce Peebles for assistance with Raman spectroscopy.

REFERENCES

ALZURIA
M.
1984
.
Nota sobre la fracción mineral en Dentalium mutabile inaequicostatum (Dautzemberg, 1891) (Mollusca, Scaphopoda)
.
Publicaciones del Deptartamento de Zoología Barcelona
 ,
10
:
23
25
.
ANDERSSON
A.J.
,
MACKENZIE
F.T.
,
BATES
N.R.
2008
.
Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers
.
Marine Ecology Progress Series
 ,
373
:
265
273
.
BØGGILD
O.B.
1930
.
The shell structure of the mollusks
.
Kongelige Danske Videnskabernes Selskabs Skrifter, Naturvidenskabelig og Mathematiske Afhandlinger
 ,
2
:
231
325
.
BROOKER
L.R.
,
SHAW
J.A.
2012
.
The chiton radula: a unique model for biomineralization studies
. In:
Advanced topics in biomineralization
  (
Seto
J.
, ed.), pp.
65
84
.
InTech Rijeka, Croatia
.
CLARKE
F.W.
,
WHEELER
W.C.
1917
.
The inorganic constituents of marine invertebrates
.
United States Geological Survey Professional Paper
 ,
102
:
1
56
.
CLARKE
F.W.
,
WHEELER
W.C.
1922
.
The inorganic constituents of marine invertebrates
.
United States Geological Survey Professional Paper
 ,
124
:
1
62
.
COUVREUR
M.
1979
.
Structure microscopique du test de quelques scaphopodes
.
Annales de L'Institut Océanographique (Paris)
 ,
7
:
199
214
.
DE PAULA
S.M.
,
SILVEIRA
M.
2009
.
Studies on molluscan shells: contributions from microscopic and analytical methods
.
Micron
 ,
40
:
669
690
.
ENGESER
T.S.
,
RIEDEL
F.
,
BANDEL
K.
1993
.
Early ontogenetic shells of Recent and fossil Scaphopoda
.
Scripta Geologica, Special Issue
 ,
2
:
83
100
.
FEELY
R.A.
,
SABINE
C.L.
,
BYRNE
R.H.
,
MILLERO
F.J.
,
DICKSON
A.G.
,
WANNINKHOF
R.
,
MURATA
A.
,
MILLER
L.A.
,
GREELEY
D.
2012
.
Decadal changes in the aragonite and calcite saturation state of the Pacific Ocean
.
Global Biogeochemical Cycles
 ,
26
:
GB3001
.
GLOVER
E.
,
TAYLOR
J.
,
WHITTAKER
J.
2003
.
Distribution, abundance and foraminiferal diet of an intertidal scaphopod, Laevidentalium lubricatum, around the Burrup Peninsula, Dampier, Western Australia
. In:
The marine flora and fauna of Dampier, Western Australia
  (
Wells
F.E.
,
Walker
D.I.
,
Jones
D.S.
, eds), pp.
225
240
.
Western Australian Museum
,
Perth
.
GRAY
B.E.
,
SMITH
A.M.
2004
.
Mineralogical variation in shells of the blackfoot abalone Haliotis iris (Mollusca: Gastropoda: Haliotidae) in southern New Zealand
.
Pacific Science
 ,
58
:
47
64
.
HABE
T.
1964
.
Fauna Japonica Scaphopoda (Mollusca)
 .
Biogeographical Society of Japan, Electrical Engineering College Press
,
Tokyo
.
LOWENSTAM
H.A.
,
WIENER
S.
1989
.
On biomineralization
 .
Oxford University Press
,
New York
.
MULCRONE
R.
2005
.
Scaphopoda. Animal Diversity Web
. .
Accessed 18 December 2011
.
NEHRKE
G.
,
NOUET
J.
2011
.
Confocal Raman microscope mapping as a tool to describe different mineral and organic phases at high spatial resolution within marine biogenic carbonates: case study on Nerita undata (Gastropoda, Neritopsina)
.
Biogeosciences
 ,
8
:
3761
3769
.
REYNOLDS
P.D.
,
OKUSU
A.
1999
.
Relationships among families of the Scaphopoda (Mollusca)
.
Zoological Journal of the Linnean Society
 ,
126
:
131
154
.
SCHRÖDL
M.
,
STÖGER
I.
2014
.
A review on deep molluscan phylogeny: old markers, integrative approaches, persistent problems
.
Journal of Natural History
 ,
48
:
2773
2804
.
SMITH
A.M.
2012
.
Argonauta at risk: dissolution and carbonate mineralogy of egg cases
. In:
Proceedings of the 12th International Coral Reef Symposium
  (
Yellowlees
D.
,
Hughes
T.P.
, eds),
Paper 8A-1
.
James Cook University
,
Cairns
.
SMITH
A.M.
,
KEY
M.M.
Jr.
,
GORDON
D.P.
2006
.
Skeletal mineralogy of bryozoans: taxonomic and temporal patterns
.
Earth-Science Reviews
 ,
78
:
287
306
.
SMITH
A.M.
,
RIEDI
M.A.
,
WINTER
D.J.
2013
.
Temperate reefs in a changing ocean: skeletal carbonate mineralogy of serpulids
.
Marine Biology
 ,
160
:
2281
2294
.
SMITH
A.M.
,
SUTHERLAND
J.E.
,
KREGTING
L.
,
FARR
T.J.
,
WINTER
D.J.
2012
.
Phylomineralogy of the coralline red algae: correlation of skeletal mineralogy with molecular phylogeny
.
Phytochemistry
 ,
81
:
97
108
.
STEINER
G.
,
KABAT
A.R.
2001
.
Catalogue of supraspecific taxa of Scaphopoda (Mollusca)
.
Zoosystema
 ,
23
:
433
460
.
STEINER
G.
,
KABAT
A.R.
2004
.
Catalog of species-group names of Recent and fossil Scaphopoda (Mollusca)
.
Zoosystema
 ,
26
:
549
726
.
TAYLOR
P.D.
,
JAMES
N.P.
,
BONE
Y.
,
KUKLINSKI
P.
,
KYSER
T.K.
2009
.
Evolving mineralogy of cheilostome bryozoans
.
Palaios
 ,
24
:
440
452
.
VOVELLE
J.
,
GRASSET
M.
1983
.
Biomineralisation des dents radulaires chez Dentalium dentalis L
.
Haliotis
 ,
13
:
123
130
.