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Salinity effects on the Mg/Ca and Sr/Ca in starfish skeletons and the
echinoderm relevance for paleoenvironmental reconstructions
Catherine Borremans1, Julie Hermans1,2, Sandrine Baillon, Luc André3, Philippe Dubois1*
1
Laboratoire de Biologie Marine (CP 160/15), Université Libre de Bruxelles, 50 avenue F.D. Roosevelt, B-1050 Brussels, Belgium
2
Département des Invertébrés, Institut Royal des Sciences Naturelles de Belgique, 29 rue Vautier, B-1000 Brussels, Belgium
3
Section de Minéralogie, Pétrographie et Géochimie, Musée Royal d’Afrique Centrale, 13 Leuvensesteenweg, B-3080 Tervuren, Belgium
ABSTRACT
Skeletal Mg/Ca ratios of well-preserved fossil echinoderms have been used to reconstruct
past Mg/Ca ratio in seawater up to the Phanerozoic, taking into account the known temperature effect on this ratio. This study investigates the effects of salinity and growth rate on
Mg/Ca and Sr/Ca ratios in starfish calcite skeletons grown in experimental conditions. Both
ratios are not related to growth rate: on the contrary, both are positively related to salinity. This
effect induces an error on the reconstructed Mg/Ca ratio in seawater that may reach 46%. An
intriguing inverse relation between skeletal Sr/Ca ratio and temperature was recorded. The
salinity effects are presumably due to physiological regulation processes.
INTRODUCTION
Echinoderms are abundant, widely distributed benthic invertebrates and their endoskeletons are generally well preserved in the
geological records. This skeleton is made of
ossicles located in the dermis. Each ossicle
consists in a three-dimensional network of
mineralized trabeculae, the stereom. Each
ossicle is composed of a single crystal of highmagnesium calcite in which Sr is the main
trace element. It also contains 0.1% organic
material (the intrastereomic organic matrix,
IOM). The skeleton is formed intracellularly
in cell processes of the skeleton-forming cells
(for a review, see Dubois and Chen, 1989). The
high-magnesium calcite phase results from the
progressive crystallization of a transient amorphous calcium carbonate phase (ACC) presumably delivered in the calcifying vacuole in the
form of ACC-containing vesicles (Wilt, 2002;
Beniash et al., 1997, 1999; Politi et al., 2004).
The Mg/Ca ratio of the skeleton is related
to temperature (Clarke and Wheeler, 1922;
Chave, 1954; Weber, 1969) and seawater Mg/Ca
ratio (Ries, 2004). Because the Mg/Ca ratio in
seawater is spatially constant and unlikely to
change on time scales of <1 m.y. due to the very
long residence times of both Mg and Ca in the
oceans, the well-preserved fossils were used
to reconstruct long-term changes in seawater
Mg/Ca ratio up to the Phanerozoic (Dickson,
2002; Ries, 2004). Ries (2004) proposed algorithms that relate skeletal and seawater Mg/Ca
ratios, taking into account the temperature effect,
to reconstruct paleoceanic Mg/Ca ratio. However, another oceanographic parameter, salinity, could also affect significantly the Mg/Ca
skeletal ratio. Previous studies reported a weak
salinity effect on the Mg incorporation into the
*E-mail: [email protected].
skeleton of field-collected echinoderms (Chave,
1954; Pilkey and Hower, 1960; Richter and
Bruckschen, 1998). However, because salinity
and temperature often covary, deconvoluting
both signals is not easy. Ferguson et al. (2008)
reported a strong salinity effect on the Mg/Ca
ratio in Mediterranean high-magnesium calcite
foraminiferal skeletons. Furthermore, Weber
(1969, 1973) argued that the incorporation
of Mg in echinoderms was mainly driven by
growth rate. However, in most taxa with calcite skeletons, it is the Sr/Ca ratio that is linked
to growth (Lorrain et al., 2005; Rickaby et al.,
2002; Stoll and Schrag, 2000). In echinoderms,
only one study was dedicated to the Sr/Ca ratio.
Pilkey and Hower (1960) showed a weak trend
between the skeletal Sr/Ca ratio and temperature in a single species collected along a latitudinal gradient, but they did not correlate it with
growth rate. In this study, we used the starfish
Asterias rubens, a euryhaline species, to determine in controlled aquarium conditions the relationships between Mg/Ca and Sr/Ca ratios in the
skeleton and salinity as well as growth rate. Possible confusing factors like animal age (size) or
ossicle type were also investigated.
MATERIAL AND METHODS
All experiments were carried out using the
starfish A. rubens. This species is able to withstand large salinity differences (Sarantchova,
2001) and is representative of echinoderm skeletal characteristics (e.g., see Dubois and Chen,
1989). Furthermore, it can be easily obtained
in large numbers and shows fast growth in an
aquarium. Materials and methods details are
available in GSA Data Repository.1
Field Samples
For analysis of Mg, Sr, and Ca in different
skeletal plates, starfish A. rubens were collected
at low tide on a breakwater in Knokke (Belgium)
on 9 January 2007. Starfish were immediately
dissected. For assessing the effect of size (age)
on Mg/Ca and Sr/Ca ratios, 92 A. rubens showing a wide range of sizes (17–105 mm ray
length) were collected at low tide on a breakwater in Audresselles (Pas-de-Calais, France)
on 26 October 2007. Starfish were measured
and then stored at −20 °C until treatment.
Experimental Study
Juvenile A. rubens (10–35 mm in ray length)
and mussels were collected in November 2006
at low tide on breakwaters in Knokke, Belgium.
Temperature and salinity at the sampling site were
12.5 °C and 31.8 psu, respectively. After acclimatization, the starfish were transferred in eight
independent closed-circuit aquariums containing 100 L of Wimereux (Pas-de-Calais, France)
seawater at 14 °C and 30 psu. The initial size
distributions of the starfish were identical in all
aquariums (median size = 28 ± 1 mm). Temperature and salinity were modified by 0.5 psu/4 days
and 1 °C/10 days to reach the experimental conditions (11, 18 °C; 25, 28, 32, 35 psu).
Once this was achieved, starfish arm length
was measured monthly and food was provided
freely, using nine different batches of mussels
from Knokke. Salinity, temperature, and pH were
measured regularly in each aquarium. Temperature and salinity conditions of the entire experiment are summarized in the Data Repository.
1
GSA Data Repository item 2009087, materials
and methods details, Table DR1 (salinity and temperature conditions), Table DR2 (data presented in
Figure 1), Figure DR1 (schematic cross section of
Asterias rubens arm), and Figure DR2 (Sr/Ca versus size relationship), is available online at www.
geosociety.org/pubs/ft2009.htm, or on request from
[email protected] or Documents Secretary,
GSA, P.O. Box 9140, Boulder, CO 80301, USA.
© 2009 The Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or [email protected].
GEOLOGY,
April
2009
Geology,
April
2009;
v. 37; no. 4; p. 351–354; doi: 10.1130/G25411A.1; 2 figures; 2 tables; Data Repository item 2009087.
351
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The newly formed parts of juvenile arms, after
four months of growth under controlled conditions (June 2007), were determined using the
monthly size measurements and the results from
a separate calcein labeling experiment. The distal newly grown parts of the starfish arms were
dissected in starfish that reached at least 41 mm
(maximum size reached was 66 mm) and were
stored at −20 °C. At the end of the experiment,
water samples were taken in triplicates from
the different systems and stored at −20 °C until
analysis. Ca consumed by the starfish for biomineralization was <1% of the initial Ca present
in the aquarium seawater. Therefore, Ca, Mg, and
Sr concentrations in the seawater could be considered as constant throughout the experiment.
Furthermore, Mg/Ca ratios in seawater of the
different aquariums were not linked to salinity
(pregression > 0.40) at the end of the experiment.
Seawater and Skeleton Analyses
For analytical methods, see the Data Repository.
RESULTS
Field Specimens
The Mg/Ca and Sr/Ca ratios were measured
in the different types of ossicles forming the
whole skeleton (adambulacral plates, adambulacral spines, ambulacral plates, aboral
plates, upper marginal plates; see the Data
Repository). Significant but weak differences
were recorded between these different plates
(pANOVA repeated measures < 10 −5) (Table 1).
The skeletal Sr/Ca ratio was significantly
dependent on the size of the starfish (Sr/Ca =
−0.0028 × size + 2.6897; R2 = 0.7812;
pregression < 10−6; see the Data Repository). On the
contrary, the size had no significant effect on the
skeletal Mg/Ca ratio (pregression = 0.061) (mean ±
standard deviation = 104 ± 8; n = 92). Over this
size range the 95% confidence interval (CI 95)
was 87–120 mmol/mol.
Experimental Study
Both temperature and salinity affected
Mg/Ca and Sr/Ca ratios in the newly formed
skeleton (Table 2). On the contrary, neither
growth rate nor final size was significantly
related to these ratios in the encompassed ranges
(Table 2). Salinity effects accounted for 25% of
the variation in Mg/Ca ratios and temperature
for a further 32%. Thus, individual variation was
responsible for 43% of the variation with CI 95
ranging between 90–98 and 94–115 mmol/mol,
i.e., 8%–22% of the mean, according to the considered conditions. It is noteworthy that the
Mg/Ca versus salinity relationships differed
according to temperature (Fig. 1A).
The Sr/Ca ratio was highly dependent on
salinity, the latter explaining 70% of the variation, temperature accounting for a further 16%
352
TABLE 1. MG/CA RATIOS IN SKELETAL
PLATES OF ASTERIAS RUBENS
Type of
Mg/Ca
Sr/Ca
calcified tissue
(mmol/mol)* (mmol/mol)*
c
2.56 ± 0.04c
Skeleton bulk
112 ± 7
Adambulacral plates
113 ± 7c
2.55 ± 0.04c
Adambulacral spines
106 ± 6b
2.50 ± 0.04a
Ambulacral plates
96 ± 4a
2.51 ± 0.04b
Aboral plates
96 ± 4a
2.51 ± 0.04a,b
Upper marginal plates
97 ± 3a
2.53 ± 0.03b
Note: Values sharing the same superscript are not
significantly different.
*Mean ± standard deviation; n = 20.
(Table 2). Sr/Ca ratios versus salinity relations
did not differ according to temperature (Fig. 1B).
Individual variation in Sr/Ca was lower, with CI 95
ranging from 2.18–2.26 to 2.25–2.42 mmol/mol,
i.e., 4%–7% of the mean.
DISCUSSION
Mg/Ca Ratio in Different Ossicle Types
In contrast to sea urchins, no strong differences of Mg/Ca ratio between ossicles were
detected in A. rubens. For example, the test of
Echinometra mathaei contains 16.2% MgCO3
(w/w) and its spines 7.5% MgCO3 (w/w) (Weber,
1969). In A. rubens, the highest magnesium
difference was found between adambulacral
plates, 9.3% MgCO3 (w/w), and ambulacral
plates, 8.0% MgCO3 (w/w). Furthermore, no
difference between oral and aboral faces and
between more or less external ossicle positions
were detected. This allows the use of the whole
starfish skeleton for the Mg/Ca ratio analyses.
Size (Age) Effect on the Mg/Ca and the
Sr/Ca Ratios
The Mg/Ca ratio is independent of the starfish
size (age), making comparisons between different populations robust.
The Sr/Ca ratio was negatively related to the
starfish size, as already shown in planktonic
foraminifera, other organisms with a highmagnesium calcite skeleton (Elderfield et al.,
2002). Growth rate is probably the mechanistic
basis of this relation. Younger (smaller) starfish
grow much faster than older ones and strontium
distribution coefficients are known to increase
with increasing precipitation rate (Lorens,
1981). On the contrary, no size effect was
detected on the Sr/Ca ratio in the skeleton of the
experimental specimens, probably because the
size range (41–66 mm ray length) was narrower
than in the field study (17–105 mm ray length)
and thus impeded to detect an effect.
Salinity Effect on Mg/Ca Ratio
Under experimental conditions, when a
wide range of salinity was used, a clear salinity effect on the Mg/Ca ratio was evidenced in
A. rubens. The salinity dependence was linear
and accounted for 0.94–1.69 (mmol/mol)/psu,
i.e., ~1% to ~1.5%/psu. These values are of
the same magnitude as the temperature effect
on the echinoderm skeleton Mg/Ca ratio, i.e.,
~2%/°C (Chave, 1954). This result is in contradiction with Richter and Bruckschen’s (1998)
field results. In their study, specimens were collected in very contrasted ecosystems (Kattegat,
North Sea, Atlantic, and Mediterranean), showing different ranges of seawater temperature that
correlated with salinity. We suggest that, in the
latter case, the salinity effect was masked by
the temperature effect and possibly by signatures of different water masses.
The salinity effect reported in the present
study was not due to differences in growth rate
depending on salinity. As seawater Mg/Ca ratio
showed no relation with salinity (see section on
Material and Methods), such an effect can also
be ruled out. Differences in Mg and Ca transport or homeostasis according to salinity could
be involved. A. rubens is an osmoconformer,
its perivisceral and ambulacral fluids being
isosmotic and isoionic with seawater, except for
Ca and K, which are regulated (Binyon, 1962;
Stickle and Diehl, 1987). If calcium uptake is at
least partly controlled, magnesium concentration
in inner fluids would vary more than calcium
ones with seawater concentrations and, thereby,
with salinity. As a consequence, the Mg/Ca ratio
of inner fluids would be lower at lower salinities.
In vitro, the Mg/Ca ratio of highly supersaturated solutions was demonstrated to define the
magnesium content of the resulting amorphous
TABLE 2. STATISTICAL RESULTS OF THE STEPWISE MULTIPLE
REGRESSIONS BETWEEN MG/CA AND SR/CA RATIOS IN THE NEWLY
FORMED SKELETON AND POSSIBLE INDEPENDENT VARIABLES
1st
variable
Mg/Ca
Salinity
Salinity
Salinity
Salinity
2nd
variable
Temperature
Temperature
Temperature
3rd
variable
Growth rate
Size
Sr/Ca
Salinity
Salinity
Temperature
Salinity
Temperature
Growth rate
Salinity
Temperature
Size
Note: R2 is coefficient of determination.
R2
Significance
of additional
variable
0.25
0.57
0.57
0.57
<10–5
<10–5
0.7
0.8
0.70
0.86
0.86
0.86
<10–5
<10–5
0.7
0.9
GEOLOGY, April 2009
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A
Mg/Ca (mmol/mol)
120
110
y = 1.6898x + 51.6829
R2 = 0.685; p = 2.2 10–5
100
90
y = 0.9443x + 65.4850
R2 = 0.395; p = 7 10–5
80
Sr/Ca (mmol/mol)
70
2.6
2.5
B
y = 0.0183x + 1.8239
R2 = 0.808; p < 10–6
2.4
2.3
2.2
y = 0.0173x + 1.7779
R2 = 0.730; p = 6 10–6
2.1
2
20
25
30
35
40
Salinity (psu)
Figure 1. A: Mg/Ca ratio (mmol/mol) in
the skeleton of Asterias rubens grown in
aquarium according to salinity and temperature of growth (+11 °C; 18 °C); equations and parameters of linear regressions
at each temperature (–11 °C; – – – 18 °C).
B: Sr/Ca ratio (mmol/mol) in the skeleton of
A. rubens grown in aquarium according to
salinity and temperature of growth (+11 °C;
18 °C); equations and parameters of the linear regressions at each temperature (–11 °C;
– – – 18 °C).
calcium carbonate (ACC) precipitate both in
the absence and presence of organic matrix-like
macromolecules (Raz et al., 2000; Loste et al.,
2003; Cheng et al., 2007; Gayathri et al., 2007).
Subsequently, ACC containing more Mg crystallized to yield calcites with higher Mg concentrations. Therefore, if in vivo mechanisms (which
also include a transient ACC phase) follow these
in vitro processes, the differential regulation of
Mg and Ca could be responsible for the observed
effect. Alternatively, salinity could induce a
modification in the composition or abundance of
the intraskeletal organic matrix, which was suggested to control the Mg content of the echinoderm skeleton (Dubois and Chen, 1989). Such
a hypothesis was already proposed by Vander
Putten et al. (2000) to account for seasonal variations in the Mg content of Mytilus edulis calcite
shell layer. Acidic organic macromolecules stabilize in vitro the transient ACC phase (Raz et al.,
2000) and possibly play an important role in the
hydration of this phase, allowing an easier incorporation of the Mg ion, which has a relatively
large dehydration barrier (Cheng et al., 2007).
Furthermore, Robach et al. (2006) demonstrated
that higher Mg concentrations in the sea urchin
tooth were linked to matrix molecules richer in
aspartic acid. Thus, one may hypothesize that
more acid matrix molecules will, in vivo, further
stabilize the transient ACC phase, allowing for a
higher incorporation of Mg.
Using Ries’ (2004) algorithms we reconstructed seawater Mg/Ca ratio and the error
induced by the salinity effect on the calcite
GEOLOGY, April 2009
Mg/Ca ratio. This induced an error in deduced
seawater Mg/Ca ratio between 2% and 5% at a
difference of 1 psu and between 16% and 46%
for a difference of 10 psu (Fig. 2), according
to the seawater Mg/Ca ratio. The highest error
occurs for the lowest seawater Mg/Ca ratio
of 1.29, i.e., values inferred for a part of the
Phanerozoic oceans (see e.g., Dickson, 2002).
This result emphasizes the need to consider the
salinity effect, with the temperature effect, when
reconstructing long-term changes (Δt > 1 m.y.)
in the seawater Mg/Ca ratio.
Temperature and Salinity Effects on
Sr/Ca Ratio
The Sr/Ca ratio in the skeleton of A. rubens
grown in experimental conditions depended
on both temperature and salinity. Higher Sr/Ca
ratios were recorded at lower temperature. This
is consistent with field results in a sand dollar,
where a linear inverse relation between Sr/Ca
ratio and temperature of the collection site was
documented (Pilkey and Hower, 1960). This
relation is unusual for biogenic calcites in which
Sr/Ca ratios are either unrelated or positively
linked to temperature (e.g., De Deckker et al.,
1999; Lea et al., 1999; Stoll et al., 2002).
Wasylenki et al. (2005) showed that Sr incorporation into abiotic calcite increased with
supersaturation. However, supersaturation in
seawater increases with temperature (Morse and
Mackenzie, 1990). Supersaturation level in the
calcifying vacuole is unknown, but metabolism
increases with temperature and a higher ion transport is expected. To our knowledge, Sr incorporation in ACC has never been investigated. Such
a study, including possible interactions and/or
competition with Mg, could provide a first
insight in the mechanisms of Sr/temperature
relationships in the echinoderm skeleton. The
thermodynamics of the process should be worth
investigating (Sr incorporation in the aragonite
lattice is exothermic and responsible for the
inverse relation between Sr concentration and
temperature in aragonitic minerals).
The Sr/Ca ratios in the starfish skeleton
increased with salinity. This relation cannot
be explained by kinetic factors, as growth rate
had no influence on the skeletal Sr/Ca ratio.
Furthermore, because the seawater Sr/Ca ratio
remains constant between 10 and 35 psu (Dodd
and Crisp, 1982; Ingram et al., 1998; Shen et al.,
1996), the variation of skeletal Sr/Ca ratio cannot be the result of variation in seawater Sr/Ca
ratios. A metabolic effect due to salinity can be
proposed, as the one deduced for Mytilus trossulus by Klein et al. (1996). In these mussels,
intracellular transport of shell-forming inorganic
components from seawater to the site of mineralization dominated intercellular transport. As
intracellular transport is more Ca specific than
intercellular transport, Ca concentration will be
Figure 2. Impact of the salinity effect on seawater Mg/Ca ratio reconstruction (%).
controlled and Sr concentration will decrease
in response to a salinity decrease. The skeletal
Sr/Ca ratio will then decrease with salinity. It
is interesting that, for echinoderms, Ca has also
been reported to be controlled in echinoderm
inner fluids (see Binyon, 1962; Stickle and
Diehl, 1987), while Sr was not.
Ion Transport in Echinoderms
Ion transports and especially the mechanisms
by which Ca is regulated, while Mg and Sr are
not, are key issues. In echinoderms, ion transport
from seawater is mediated by pumps and channels (see Dubois and Chen, 1989, for a review).
Seawater vacuolization as shown in foraminifera (Erez, 2003) has never been reported in the
numerous transmission electron microscopy
studies carried out on the integument or tube
feet of echinoderms (for a review, see Harrison
and Chia, 1994). Furthermore, these studies
clearly showed belted desmosomes linking epidermal cells, and making an intercellular pathway through the epidermis very unlikely (Carré
et al., 2006). Seawater can enter the water vascular system of the echinoderms through the
madreporite, but no evidence of further translocation of seawater through the epithelium lining
of this system has ever been reported.
CONCLUSION
A salinity effect on Asterias rubens skeletal
Mg/Ca and Sr/Ca ratios was evidenced under
experimental conditions: it accounted for 0.94–
1.69 (mmol/mol)/psu and 0.02 (mmol/mol)/psu,
respectively. This effect induces an error on the
reconstructed seawater Mg/Ca that may account
for as much as 46% according to the seawater
Mg/Ca ratio. Consequently, salinity should not
be overlooked when reconstructing seawater
Mg/Ca ratio from echinoderm calcite Mg/Ca
ratio. The salinity effect on Sr/Ca ratio is well
constrained and would deserve a verification in
the field. The salinity effect on both Mg/Ca and
Sr/Ca ratios seems to be due to the physiological
regulation of the Ca ion (and not of Mg and Sr
ions) in inner fluids rather than to thermodynamic
or kinetic factors as suggested in other taxa.
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ACKNOWLEDGMENTS
We thank anonymous reviewers for fruitful suggestions and Jacques Navez, Laurence Monin, and
Nourdine Dakhani for the very helpful contributions
to specimen analyses. This project was supported by
the Belgian Federal Science Policy Office, contract
SD/CS/02A, and by the National Fund for Scientific
Research (contract 2.4532.07) (NFSR, Belgium).
P. Dubois is a Senior Research Associate of the NFSR
and J. Hermans is holder of a “plan Action II ” doctoral
grant from the Belgian Federal Science Policy Office.
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Manuscript received 6 August 2008
Revised manuscript received 26 November 2008
Manuscript accepted 1 December 2008
Printed in USA
GEOLOGY, April 2009
Downloaded from geology.gsapubs.org on July 7, 2015
Geology
Salinity effects on the Mg/Ca and Sr/Ca in starfish skeletons and the
echinoderm relevance for paleoenvironmental reconstructions
Catherine Borremans, Julie Hermans, Sandrine Baillon, Luc André and Philippe Dubois
Geology 2009;37;351-354
doi: 10.1130/G25411A.1
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