Chung, P.

Cuif, J.P.

Cusack, M.

Dauphin, Y.

Parkinson, D.

Perez-Huerta, A.

English

Enlighten: Publications

 
 
 
 
 
 
 
Cusack, M. and Perez-Huerta, A. and Chung, P. and Parkinson, D. and 
Dauphin, Y. and Cuif, J.P. (2008) Oxygen isotope equilibrium in 
brachiopod shell fibres in the context of biological control. Mineralogical 
Magazine, 72 (1). pp. 239-242. ISSN 0026-461X 
 
http://eprints.gla.ac.uk/24371/ 
 
Deposited on: 21 December 2009 
 
 
Enlighten – Research publications by members of the University of Glasgow 
http://eprints.gla.ac.uk 
Oxygen isotope equilibrium in brachiopod shell fibres
in the context of biological control
M. CUSACK1,*, A. PE´REZ-HUERTA1, P. CHUNG1, D. PARKINSON3, Y. DAUPHIN2 AND J.-P. CUIF2
1 Department of Geographical and Earth Sciences, University of Glasgow, UK
2 UMR IDES 8148, Bat 504, Universite´ Paris XI-Orsay, F-91405 Orsay Cedex, France
3 Donaldon Associates Ltd., The Pentagon Centre, 36 Washington St, Glasgow, UK
Introduction
WITH their long geological history and stable low-
Mg calcite shells, Rhynchonelliform brachiopods
are attractive sources of environmental data such
as past seawater temperature (Buening and Spero,
1996; Auclair et al., 2003; Brand et al., 2003;
Parkinson et al., 2005). Concerns about the
influence of vital effects on the stable isotope
composition of brachiopod shells (Popp et al.,
1986), led to isotope analyses of different parts of
brachiopod shells in order to identify those parts
of the shell that are influenced by any vital effect
and those parts that may be suitable recorders of
seawater temperature via stable oxygen isotope
composition (Carpenter and Lohmann, 1995;
Parkinson et al., 2005). Such detailed studies
demonstrated that the outer primary layer of
acicular calcite is isotopically light in both d18O
and d13C while the secondary layer, composed of
calcite fibres, is in oxygen-isotope equilibrium
with ambient seawater (Fig. 1) (Parkinson et al.,
2005). Use of the isotopically-light primary layer
calcite in temperature calculations would result in
seawater temperatures that are significantly higher
than the actual ambient seawater temperature
(Parkinson et al., 2005). Isotopic equilibrium
between ambient seawater and secondary layer
calcite is attained while biological processes exert
strict control on all aspects of shell formation.
This biological control is evident in the
morphology and juxtaposition of the calcite
fibres; each has a diameter of ~10 mm and the
fibre length is parallel to the shell exterior.
Detailed analyses of brachiopod shell calcite
fibres, using electron back-scatter diffraction
(EBSD) and atomic force microscopy (AFM),
reveal the extent of the biological control.
Results and discussion
The calcite fibres of the secondary layer are
parallel to the shell exterior. Electron backscatter
diffraction (EBSD) reveals that the fibres are
effectively single crystals with the calcite c axis
perpendicular to the fibre axis (Fig. 2) (Schmahl
et al., 2004; Cusack et al., 2007). Thus, as fibres
grow, the crystallographic orientation of each
fibre is maintained. The granular nature of the
fibres is evident in the AFM images (Fig. 3)
where the addition of bands of calcite granules to
the growing fibre is clear. These bands of granules
are thus added over the duration of fibre growth
with uniform crystallographic orientation. The
calcite fibres of Rhynchonelliform brachiopods
* E-mail: Maggie.Cusack@ges.gla.ac.uk
DOI: 10.1180/minmag.2008.072.1.239
Mineralogical Magazine, February 2008, Vol. 72(1), pp. 239–242
# 2008 The Mineralogical Society
FIG. 1. d18Od13C crossplot of Calloria inconspicua.
are not unique in terms of biomineral structures
composed of nano-granules that collectively form
what are essentially single crystals.
This phenomenon occurs in other biogenic
carbonate structures such as tablets of aragonite
nacre (Rousseau et al., 2005; Addadi et al., 2006;
Nudelman et al., 2007) and calcite prisms in
molluscs (Nudelman et al., 2007). Such granules
occur in many phyla and, overall, the size range is
constrained (Dauphin et al., 2007). The aragonite
granules of the cephalopod Nautilus are 4050
nm in diameter (Dauphin et al., 2007). Granules
of similar dimensions to those of Nautilus,
comprise the calcite prismatic layer of Pinna
and Pinctada (Bivalvia) (Dauphin, 2003) and the
aragonite crossed lamellar layers and calcite
prisms of Concholepas and Haliotis (Dauphin,
2003). Such granules are also present in the
aragonite skeletons of Scleractinia corals (Cuif
and Dauphin, 2005: Dauphin, 2006) and in the
calcite skeletons of Octocorallia (Dauphin, 2006).
These granules in T. retusa are 600 nm long
and therefore larger than in other calcium
carbonate biominerals. The factors that determine
the dimension of the granules are unknown. The
shape of the brachiopod granules are also
different form those of mollusc shells or coral
skeletons. Brachiopod granules are more trian-
gular than those of molluscs or corals, and the
sharp end of a granule is inserted in the hollow
large part of the underlying granule (Fig. 4b). The
large size and indeed shape of T. retusa calcite
granules is intriguing and it remains to be
determined whether or not this is a general
feature of brachiopod calcite or unique to T.
retusa. It raises the question of what factors
determine the size of granules and why brachio-
pods, or T. retusa at least, should have larger
granules than those in other calcite and aragonite
biominerals.
FIG. 3. Low magnification AFM images of a polished and etched section of T. retusa shell. (a) Low magnification
height image showing the juxtaposition of several fibres separated by thin zones (arrows). (b) Phase image of the
same zone, which shows the fibre margins (dark zone) have different physical and/or chemical properties relative to
the inner part of the fibres. (c) Height image showing the detail of a fibre, with the granular structure and growth lines
(arrows) clearly visible.
FIG. 2. Crystallographic orientation map of calcite fibres
of T. retusa shell. Crystallographic orientation indicated
by the colour key. This indicates that the calcite plane is
normal to the field of view. White wire frames indicate
the orientation of the unit cell. The outer (primary layer)
and shell exterior are to the top of the image (not
shown). Scale bar = 50 mm.
240
M. CUSACK ET AL.
Conclusions
The extent of the biological control exerted on the
formation of the hierarchical structure of the
calcite fibres is evident. The shape and dimen-
sions of the granules are constrained as is their
crystallographic alignment within the fibres. The
dimensions and orientations of the fibres are also
well constrained. Although there remains much to
be understood about how this precise biological
control is achieved, the attainment of isotope
equilibrium under such strict biological influence
is counter-intuitive.
Acknowledgements
MC and APH gratefully acknowledge financial
support from the BBSRC (BB/E003265/1). MC
also acknowledges support from BBSRC/EPSRC
(BB/E025110/1). DP thanks the University of
Glasgow for a Nielsen Scholarship. Support from
the European Science Foundation (ESF) under the
EUROCORES Programme EuroMinScI
(BIOCALC project), through contract No.
ERAS-CT-2003-980409 of the European
Commission, DG Research, FP6, is acknowl-
edged. This work is in keeping with the aims of
Theme 3 of the Scottish Alliance for Geoscience,
Environment and Society (SAGES).
References
Addadi, L., Joester, D., Nudelman, F. and Weiner, S.
(2006) Mollusk shell formation: A source of new
concepts for understanding biomineralization pro-
cesses. Chemistry  A European Journal, 12,
981987.
Auclair, A.-C., Joachimski, M.M. and Le´cuyer, C.
(2003) Deciphering kinetic, metabolic and environ-
mental controls on stable isotope fractions between
seawater and the shell of terebratalia transversa
(brachiopoda). Chemical Geology, 202, 5978.
Brand, U., Logan, A., Hiller, N. and Richardson, J.
(2003) Geochemistry of modern brachiopods:
Applications and implications for oceanography
and paleoceanography. Chemical Geology, 198,
305334.
Buening, N. and Spero, H.J. (1996) Oxygen- and
carbon-isotope analyses of the articulate brachiopod
laqueus californianus: A recorder of environmental
change in the subeuphotic zone. Marine Biology,
127, 105114.
Carpenter, S.J. and Lohmann, K.C. (1995) D18O and
d13C values of modern brachiopod shells.
Geochimica et Cosmochimica Acta, 59, 37483764.
Cuif, J.P. and Dauphin, Y. (2005) The environment
recording unit in coral skeletons  a synthesis of
structural and chemical evidences for a biochemi-
cally driven, stepping-growth process in fibres.
Biogeosciences, 2, 6173.
Cusack, M., Perez-Huerta, A. and Dalbeck, P. (2007)
Common crystallographic control in calcite biomi-
neralization of bivalve shells. CrystEngComm, 9,
12151218.
Dauphin, Y. (2003) Soluble organic matrices of the
calcitic prismatic shell layers of two pteriomorphid
bivalves  pinna nobilis and pinctada margaritifera.
Journa l o f B io log i ca l Chemi s t r y , 278 ,
1516815177.
Dauphin, Y. (2006) Mineralizing matrices in the skeletal
axes of two corallium species (alcyonacea).
Comparative Biochemistry and Physiology, A145,
5464.
Dauphin, Y., Cusack, M. and Ortlieb. (2007)
Nanogranules in carbonate skeletons; a universal
scheme? Geophysical Research Abstracts, 9,
#02261.
Nudelman, F., Chen, H.H., Goldberg, H.A., Weiner, S.
and Addadi, L. (2007) Spiers memorial lecture:
Lessons from biomineralization: Comparing the
growth strategies of mollusc shell prismatic and
nacreous layers in atrina rigida. Faraday
FIG. 4. (a) Three dimensional AFM images of T. retusa fibres; and (b) constituent granules.
O ISOTOPE EQUILIBRIUM IN BRACHIOPOD SHELL FIBRES
241
Discussions, 136, 925.
Parkinson, D., Curry, G.B., Cusack, M. and Fallick, A.E.
(2005) Shell structure, patterns and trends of oxygen
and carbon stable isotopes in modern brachiopod
shells. Chemical Geology, 219, 193235.
Popp, B.N., Anderson, T.F. and Sandberg, P.A. (1986)
Brachiopods as indicators of original isotopic
compositions in some paleozoic limestones.
Geological Society of America Bulletin, 97,
12621269.
Rousseau, M., Lopez, E., Stemplfle, P., Brendle, M.,
Franke, L., Guette, A., Naslain, R. and Bourrat, X.
(2005) Multiscale structure of sheet nacre.
Biomaterials, 26, 62546262.
Schmahl, W.W., Griesshaber, E., Neuser, R., Lenze, A.,
Job, R. and Brand, U. (2004) The microstructure of
the fibrous layer of terebratulide brachiopod shell
calcite. European Journal of Mineralogy, 16,
693697.
242
M. CUSACK ET AL.


Oxygen isotope equilibrium in brachiopod shell fibres in the context of biological control

Enlighten

       Cusack, M. and Perez-Huerta, A. and Chung, P. and Parkinson, D. and Dauphin, Y. and Cuif, J.P. (2008) Oxygen isotope equilibrium in brachiopod shell fibres in the context of biological control. Mineralogical Magazine, 72 (1). pp. 239-242. ISSN 0026-461X  http://eprints.gla.ac.uk/24371/  Deposited on: 21 December 2009   Enlighten – Research publications by members of the University of Glasgow http://eprints.gla.ac.uk Oxygen isotope equilibrium in brachiopod shell fibresin the context of biological controlM. CUSACK1,*, A. PE´REZ-HUERTA1, P. CHUNG1, D. PARKINSON3, Y. DAUPHIN2 AND J.-P. CUIF21 Department of Geographical and Earth Sciences, University of Glasgow, UK2 UMR IDES 8148, Bat 504, Universite´ Paris XI-Orsay, F-91405 Orsay Cedex, France3 Donaldon Associates Ltd., The Pentagon Centre, 36 Washington St, Glasgow, UKIntroductionWITH their long geological history and stable low-Mg calcite shells, Rhynchonelliform brachiopodsare attractive sources of environmental data suchas past seawater temperature (Buening and Spero,1996; Auclair et al., 2003; Brand et al., 2003;Parkinson et al., 2005). Concerns about theinﬂuence of vital effects on the stable isotopecomposition of brachiopod shells (Popp et al.,1986), led to isotope analyses of different parts ofbrachiopod shells in order to identify those partsof the shell that are inﬂuenced by any vital effectand those parts that may be suitable recorders ofseawater temperature via stable oxygen isotopecomposition (Carpenter and Lohmann, 1995;Parkinson et al., 2005). Such detailed studiesdemonstrated that the outer primary layer ofacicular calcite is isotopically light in both d18Oand d13C while the secondary layer, composed ofcalcite ﬁbres, is in oxygen-isotope equilibriumwith ambient seawater (Fig. 1) (Parkinson et al.,2005). Use of the isotopically-light primary layercalcite in temperature calculations would result inseawater temperatures that are signiﬁcantly higherthan the actual ambient seawater temperature(Parkinson et al., 2005). Isotopic equilibriumbetween ambient seawater and secondary layercalcite is attained while biological processes exertstrict control on all aspects of shell formation.This biological control is evident in themorphology and juxtaposition of the calciteﬁbres; each has a diameter of ~10 mm and theﬁbre length is parallel to the shell exterior.Detailed analyses of brachiopod shell calciteﬁbres, using electron back-scatter diffraction(EBSD) and atomic force microscopy (AFM),reveal the extent of the biological control.Results and discussionThe calcite ﬁbres of the secondary layer areparallel to the shell exterior. Electron backscatterdiffraction (EBSD) reveals that the ﬁbres areeffectively single crystals with the calcite c axisperpendicular to the ﬁbre axis (Fig. 2) (Schmahlet al., 2004; Cusack et al., 2007). Thus, as ﬁbresgrow, the crystallographic orientation of eachﬁbre is maintained. The granular nature of theﬁbres is evident in the AFM images (Fig. 3)where the addition of bands of calcite granules tothe growing ﬁbre is clear. These bands of granulesare thus added over the duration of ﬁbre growthwith uniform crystallographic orientation. Thecalcite ﬁbres of Rhynchonelliform brachiopods* E-mail: Maggie.Cusack@ges.gla.ac.ukDOI: 10.1180/minmag.2008.072.1.239Mineralogical Magazine, February 2008, Vol. 72(1), pp. 239–242# 2008 The Mineralogical SocietyFIG. 1. d18Od13C crossplot of Calloria inconspicua.are not unique in terms of biomineral structurescomposed of nano-granules that collectively formwhat are essentially single crystals.This phenomenon occurs in other biogeniccarbonate structures such as tablets of aragonitenacre (Rousseau et al., 2005; Addadi et al., 2006;Nudelman et al., 2007) and calcite prisms inmolluscs (Nudelman et al., 2007). Such granulesoccur in many phyla and, overall, the size range isconstrained (Dauphin et al., 2007). The aragonitegranules of the cephalopod Nautilus are 4050nm in diameter (Dauphin et al., 2007). Granulesof similar dimensions to those of Nautilus,comprise the calcite prismatic layer of Pinnaand Pinctada (Bivalvia) (Dauphin, 2003) and thearagonite crossed lamellar layers and calciteprisms of Concholepas and Haliotis (Dauphin,2003). Such granules are also present in thearagonite skeletons of Scleractinia corals (Cuifand Dauphin, 2005: Dauphin, 2006) and in thecalcite skeletons of Octocorallia (Dauphin, 2006).These granules in T. retusa are 600 nm longand therefore larger than in other calciumcarbonate biominerals. The factors that determinethe dimension of the granules are unknown. Theshape of the brachiopod granules are alsodifferent form those of mollusc shells or coralskeletons. Brachiopod granules are more trian-gular than those of molluscs or corals, and thesharp end of a granule is inserted in the hollowlarge part of the underlying granule (Fig. 4b). Thelarge size and indeed shape of T. retusa calcitegranules is intriguing and it remains to bedetermined whether or not this is a generalfeature of brachiopod calcite or unique to T.retusa. It raises the question of what factorsdetermine the size of granules and why brachio-pods, or T. retusa at least, should have largergranules than those in other calcite and aragonitebiominerals.FIG. 3. Low magniﬁcation AFM images of a polished and etched section of T. retusa shell. (a) Low magniﬁcationheight image showing the juxtaposition of several ﬁbres separated by thin zones (arrows). (b) Phase image of thesame zone, which shows the ﬁbre margins (dark zone) have different physical and/or chemical properties relative tothe inner part of the ﬁbres. (c) Height image showing the detail of a ﬁbre, with the granular structure and growth lines(arrows) clearly visible.FIG. 2. Crystallographic orientation map of calcite ﬁbresof T. retusa shell. Crystallographic orientation indicatedby the colour key. This indicates that the calcite plane isnormal to the ﬁeld of view. White wire frames indicatethe orientation of the unit cell. The outer (primary layer)and shell exterior are to the top of the image (notshown). Scale bar = 50 mm.240M. CUSACK ET AL.ConclusionsThe extent of the biological control exerted on theformation of the hierarchical structure of thecalcite ﬁbres is evident. The shape and dimen-sions of the granules are constrained as is theircrystallographic alignment within the ﬁbres. Thedimensions and orientations of the ﬁbres are alsowell constrained. Although there remains much tobe understood about how this precise biologicalcontrol is achieved, the attainment of isotopeequilibrium under such strict biological inﬂuenceis counter-intuitive.AcknowledgementsMC and APH gratefully acknowledge ﬁnancialsupport from the BBSRC (BB/E003265/1). MCalso acknowledges support from BBSRC/EPSRC(BB/E025110/1). DP thanks the University ofGlasgow for a Nielsen Scholarship. Support fromthe European Science Foundation (ESF) under theEUROCORES Programme EuroMinScI(BIOCALC project), through contract No.ERAS-CT-2003-980409 of the EuropeanCommission, DG Research, FP6, is acknowl-edged. This work is in keeping with the aims ofTheme 3 of the Scottish Alliance for Geoscience,Environment and Society (SAGES).ReferencesAddadi, L., Joester, D., Nudelman, F. and Weiner, S.(2006) Mollusk shell formation: A source of newconcepts for understanding biomineralization pro-cesses. Chemistry  A European Journal, 12,981987.Auclair, A.-C., Joachimski, M.M. and Le´cuyer, C.(2003) Deciphering kinetic, metabolic and environ-mental controls on stable isotope fractions betweenseawater and the shell of terebratalia transversa(brachiopoda). Chemical Geology, 202, 5978.Brand, U., Logan, A., Hiller, N. and Richardson, J.(2003) Geochemistry of modern brachiopods:Applications and implications for oceanographyand paleoceanography. Chemical Geology, 198,305334.Buening, N. and Spero, H.J. (1996) Oxygen- andcarbon-isotope analyses of the articulate brachiopodlaqueus californianus: A recorder of environmentalchange in the subeuphotic zone. Marine Biology,127, 105114.Carpenter, S.J. and Lohmann, K.C. (1995) D18O andd13C values of modern brachiopod shells.Geochimica et Cosmochimica Acta, 59, 37483764.Cuif, J.P. and Dauphin, Y. (2005) The environmentrecording unit in coral skeletons  a synthesis ofstructural and chemical evidences for a biochemi-cally driven, stepping-growth process in ﬁbres.Biogeosciences, 2, 6173.Cusack, M., Perez-Huerta, A. and Dalbeck, P. (2007)Common crystallographic control in calcite biomi-neralization of bivalve shells. CrystEngComm, 9,12151218.Dauphin, Y. (2003) Soluble organic matrices of thecalcitic prismatic shell layers of two pteriomorphidbivalves  pinna nobilis and pinctada margaritifera.Journa l o f B io log i ca l Chemi s t r y , 278 ,1516815177.Dauphin, Y. (2006) Mineralizing matrices in the skeletalaxes of two corallium species (alcyonacea).Comparative Biochemistry and Physiology, A145,5464.Dauphin, Y., Cusack, M. and Ortlieb. (2007)Nanogranules in carbonate skeletons; a universalscheme? Geophysical Research Abstracts, 9,#02261.Nudelman, F., Chen, H.H., Goldberg, H.A., Weiner, S.and Addadi, L. (2007) Spiers memorial lecture:Lessons from biomineralization: Comparing thegrowth strategies of mollusc shell prismatic andnacreous layers in atrina rigida. FaradayFIG. 4. (a) Three dimensional AFM images of T. retusa ﬁbres; and (b) constituent granules.O ISOTOPE EQUILIBRIUM IN BRACHIOPOD SHELL FIBRES241Discussions, 136, 925.Parkinson, D., Curry, G.B., Cusack, M. and Fallick, A.E.(2005) Shell structure, patterns and trends of oxygenand carbon stable isotopes in modern brachiopodshells. Chemical Geology, 219, 193235.Popp, B.N., Anderson, T.F. and Sandberg, P.A. (1986)Brachiopods as indicators of original isotopiccompositions in some paleozoic limestones.Geological Society of America Bulletin, 97,12621269.Rousseau, M., Lopez, E., Stemplﬂe, P., Brendle, M.,Franke, L., Guette, A., Naslain, R. and Bourrat, X.(2005) Multiscale structure of sheet nacre.Biomaterials, 26, 62546262.Schmahl, W.W., Griesshaber, E., Neuser, R., Lenze, A.,Job, R. and Brand, U. (2004) The microstructure ofthe ﬁbrous layer of terebratulide brachiopod shellcalcite. European Journal of Mineralogy, 16,693697.242M. CUSACK ET AL.

Brachiopods as indicators of original isotopic compositions in some paleozoic limestones.

Common crystallographic control in calcite biomineralization of bivalve shells.

D 18O and d 13C values of modern brachiopod shells.

Deciphering kinetic, metabolic and environmental controls on stable isotope fractions between seawaterand the shell of terebratalia transversa (brachiopoda). Chemical Geology,

Geochemistry of modern brachiopods: Applications and implications foroceanogr aphy and paleoceanography.

Mineralizing matrices in the skeletal axes of two corallium species (alcyonacea). Comparative Biochemistry and Physiology,

Mollusk shell formation: A source of new concepts for understanding biomineralization processes.

Multiscale structure of sheet nacre.

Nanogranules in carbonate skeletons; a universal scheme?

Oxygen- and carbon-isotope analyses of the articulate brachiopod laqueus californianus: A recorder of environmental change in the subeuphotic zone.

Shell structure, patterns and trends of oxygen and carbon stable isotopes in modern brachiopod shells.

Soluble organic matrices of the calcitic prismatic shell layers of two pteriomorphid bivalves  pinna nobilis and pinctada margaritifera.

Spiers memorial lecture: Lessons from biomineralization: Comparing the growth strategies of mollusc shell prismatic and nacreous layers in atrina rigida.

The environment recording unit in coral skeletons  a synthesis of structural and chemical evidences for a biochemically driven, stepping-growth process in ﬁbres.

The microstructure of the ﬁbrous layer of terebratulide brachiopod shell calcite.

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Oxygen isotope equilibrium in brachiopod shell fibres in the context of biological control

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