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Assessing cockle shells (Anadara granosa) for reconstruction subdaily
environmental parameters: Implication for paleoclimate studies
Article in Historical Biology · June 2015
DOI: 10.1080/08912963.2015.1052806
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Assessing cockle shells (Anadara granosa) for
reconstruction subdaily environmental parameters:
Implication for paleoclimate studies
a
a
M.-Reza Mirzaei & Aileen Tan Shau Hwai
a
Marine Sciences Laboratory, School of Biological Sciences, Universiti Sains Malaysia, 11800
Minden, Penang, Malaysia
Published online: 19 Jun 2015.
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To cite this article: M.-Reza Mirzaei & Aileen Tan Shau Hwai (2015): Assessing cockle shells (Anadara granosa) for
reconstruction subdaily environmental parameters: Implication for paleoclimate studies, Historical Biology: An International
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Historical Biology, 2015
http://dx.doi.org/10.1080/08912963.2015.1052806
Assessing cockle shells (Anadara granosa) for reconstruction subdaily environmental parameters:
Implication for paleoclimate studies
M.-Reza Mirzaei* and Aileen Tan Shau Hwai
Marine Sciences Laboratory, School of Biological Sciences, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia
(Received 20 April 2015; accepted 15 May 2015)
This study aims to investigate the potential of cockle shells as an environmental recorder, examining the environmental
factors controlling the shell growth of the intertidal Anadara granosa from west coast of Malaysia. Subdaily environmental
factors were recorded from December 2011 to November 2012. A total of 600 individuals were collected on a monthly basis
and the shells sectioned from umbo to ventral margin, polished, etched and photographed under a light microscope to
observe microgrowth bands and increments. Comparison of correlation matrix between mean increment width and each
environmental factor indicated that shell growth had the highest positive correlation with seawater temperature (þ 0.72) and
weak positive correlation with salinity (þ0.53). Multiple regression analysis was used to assess independent associations
between shell mean increment width and environmental parameters. Study model showed that 60.8% of the variation in shell
growth could be explained by temperature, salinity, rainfall and tidal change. Individually, temperature and salinity made the
greatest unique contribution to explain shell growth, respectively ( p , 0.01). Laboratory results showed shell growth was in
a linear trend to optimum temperature and salinity. These findings provide a basis for the interpretation of the temporal
changes in shell microgrowth patterns in terms of environmental conditions of cockle shells.
Keywords: growth pattern; shell microgrowth increments; intertidal; temperature; salinity; shell cross section
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1.
Introduction
The reconstruction of environmental factors and life
history characteristics in invertebrates that produce
accretionary skeletons is a valuable exploration in
biological studies. Bivalves are widely distributed in
different geographical latitudes and their shells are able to
record environmental factors with high resolution.
Recently, many paleoecological studies have investigated
the effects of environmental factors on shell growth with
high accuracy using the shell growth bands of molluscs
(Brock & Bourget 1989; Richardson 1989; Goodwin et al.
2001; Schöne et al. 2006).
The cockle, Anadara granosa is a widespread species
with the highest distribution throughout South East Asia,
especially in the strait Malacca between the west coast of
Malaysia and Indonesia (Mirzaei et al. 2014a). Anadara
granosa is a suitable species to study the relationship
between shell growth and environmental parameters based
on microgrowth bands and increment widths (Richardson
1987).
Growth rate depending on these types of periodic
bands is generally associated with regional and local
environmental conditions. Therefore, mollusc shells can
be a remarkable archive of past climatic changes (Gibson
et al. 2001; Schöne et al. 2003).
Bivalve growth can be affected by several environmental parameters such as seawater temperature, salinity
and food availability (Yaroslavtseva & Sergeeva 2006;
*Corresponding author. Email: mirzaei.mr@gmail.com
q 2015 Taylor & Francis
Matozzo & Marin 2011). Sato (1999) that showed shell
microgrowth bands were affected by periodic changes in
food availability, while recent researchers have found that
food availability is dependant on tidal change (Simpson &
Sharples 2012) and emersion period (Cerrato et al. 1991).
Furthermore, geographical and temporal variations are one
of the main factors which effect shell growth at different
latitudes due to different temperatures (Wanink & Zwarts
1993; Mirzaei et al. 2014b). Variations in minerals and the
structure of growth bands are thus potential recorders of
different environmental factors, such as salinity, light and
dark periods, water current, rainfall, dissolved oxygen, pH
and suspended sediments (Marchitto Jr et al. 2000; Epplé
et al. 2006).
Most studies on molluscs used external shell layer
have focused on morphological examination (Selin 2000),
pigments (Kozminsky & Lezin 2007) and chemical
structure (Gillikin et al. 2005; Mubiana & Blust 2007).
Only a few studies have used the shell cross sections as
proxies for environmental factors (Richardson et al. 1980).
The major problem with this method was the effects of
environmental factors such as seawater temperature, tidal
change and salinity on the shell growth at the same time.
As a result, there was an overlap between all
environmental factors affecting shell growth. However,
examinations in the current study were conducted on
microgrowth bands and increments of the cockle shells
which were produced during tidal changes. This
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M.-R. Mirzaei and A.T. Shau Hwai
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Figure 1.
Location of study site, Penang Island, west coast of Malaysia.
investigation was based on marked and recovered samples.
In order to determine the effects of environmental
parameters on the shell growth of Anadara granosa,
shell increment widths were compared with environmental
parameters in Penang Island, Malaysia. The multivariate
technique was used to interpret the data and determine the
relationship between shell growth and different independent variables. A standard multiple regression was used to
show how much the variance in the dependent variable
(increment width) could be explained by independent
variables (environmental parameters). This method also
demonstrated how much unique variance in the dependent
variable could be explained by each of the independent
variables. Therefore, the main objectives of this study
were (1) to investigate the relationship between shell
Figure 2. Cutting direction from Umbo to ventral margin along
the maximum growth line.
microgrowth patterns and daily environmental variables in
Anadara granosa cockles and (2) to determine which
environmental variable was the most prominent among the
factors affecting the shell growth of Anadara granosa from
Penang Island, Malaysia.
2. Material and methods
2.1 Site preparation and sample collection
A total of 600 similar age (< 4 months) and size
(< 10 mm) Anadara granosa were stained with shell dye
(Alizarin Red) at a concentration of 30 ppm before being
transferred to the study site. The staining technique was
designed to date-mark one or more bands in the shell
structure so that subsequent growth could be related to the
staining point. Cockles were placed in a plastic mesh cage
(1.5 m £ 1.5 m £ 2 m) located at an intertidal site
(58300 05.5000 N 1008110 35.3200 E), where it could easily
be accessed by boat from Balik Pulau in Penang Island,
Malaysia (Figure 1). A total of 40 individuals of Anadara
granosa were collected monthly (40 individuals £
12 months) between December 2011 and November
2012. In the laboratory, soft tissues were gently removed
from inside the shell. A single valve of each specimen was
rinsed and numbered for shell cross section preparation.
Furthermore, a total of 25 samples of Anadara granosa
were collected fortnightly between mid-December 2011
and the end of January 2012 (4 sample collections £
25 individuals £ 1 site).
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2.2 Shell cross section preparation
Radial cross sections were prepared from one valve of any
specimen based on standard methods by Neves and Moyer
(1988). The valve of each specimen was marked by a
pencil from the umbo to the ventral margin along the
maximum growth band at a point from the shell posterior
(Figure 2). Marked valves were embedded in an epoxy
resin (a combination of epoxy resin to epoxy hardener with
the proportion of 2:1) for 24 h to protect the valves against
cutting and grinding procedures.
Valve resin mouldings were then fixed on the low speed
saw with a diamond-impregnated blade (Buehler Ltd, Lake
Bluff, IL, USA). A low speed made it possible to cut fragile
materials that would otherwise fracture. The valves were cut
through the pencil mark from the umbo to shell ventral
margin. Shell sections were then grounded by sequential grit
sandpapers (240, 400, 600, 800 and 1200 Buehler
carborundum grits) to remove epoxy resin from the cut
surfaces of the valves. The finer grits (800 and 1200) were
used to reduce scratches from the coarser grit papers. T-cut
valve surfaces were polished with Aluminum oxide powder
on a semi automatic polishing machine (FORCIMAT –
FORCIPOL 300-1V). The specimen was then removed,
rinsed in tap water and dried. Etching was conducted so as to
leave the aragonite granules on the surface of the valve
section that distort the section image. As a result, the polished
surfaces of the valves were etched by immersing the
specimens in a dilute solution of hydrochloric acid (0.1%
HCl) for 1 min.
2.3 Growth patterns periodicity
The experiment was designed to examine whether tidal
change, emersion and daily rhythms had any effect on the
shell banding formation in Anadara granosa. The total
number of growth bands was counted in each shell between
the staining point and the shell margin. A sample t test was
used to test whether the banding was daily, tidal or produced
by emersion. The mean difference between pairs of
expected and observed values was used to determine
whether the values differed significantly from zero.
2.4 Increment width measurement
The etched surface of each section was observed with light
microscope-stereo (Olympus SZ61 – Olympus Optical
Co. Ltd, Tokyo, Japan) at 100 £ magnification and
photographed (Xcam Alpha-The imaging source GmbH).
Based on Alizarin red staining on the shell, in each sample
collections the microgrowth increments were successively
measured from the shell margin toward staining point
using microscopic image analysis software (Analysis
Image Processing Version 5.1 – @Olympus soft imaging
solutions 1989 –2008).
3
2.5 Environmental data
Daily seawater temperature was measured using HOBO
Pendant Temp/Light logger fixed to the cage in the study area.
The logger was calibrated to record hourly seawater
temperatures during the experiment. Seawater salinity was
measured daily with a hand-held refractometer (RHSN10ATC BUILT) at the study site. Rainfall measurements were
recorded to the nearest 0.1 millimetre with the daily
measurements taken by Penang Island Regional Meteorological Office. Monthly tide tables of the sampling site were
obtained from Tide Tables Malaysia (2011–2012) published
by the National Hydrographica Centre, Royal Malaysian Navy.
2.6 Laboratory experiment
A total of 160 individuals of Anadara granosa were stained
using Alizarin red combined in seawater for 24 h (Riascos
et al. 2007). Factorial design (A 4 £ 3) was conducted to
compare the effects of four different temperatures (25, 27, 30
and 328C) and three salinity treatments (26, 28 and 31 ppt) on
the shell increment growth. Treatment levels fall within the
natural range of temperature and salinity in the distributional
range of the cockles in study site. The system consists of 50-l
tanks including optional water controller to produce simple
tidal fluctuations. Water was emptied every 11 h and cockles
were exposed for 1 h and then replacing with water of
appropriate salinity. Throughout the 30-day experimental
period, the cockles were fed daily with marine microalgae.
At the end of experiment, cockles were collected from each
tank, labelled and shell sections were prepared from each
group. The shell increment widths were measured from the
staining point to the last increment in shell margin.
2.7
Statistical analysis
The SPSS (Statistical programme for social scientist) software
(IBM SPSS statistics version 20) was used to analyse data
from the shell increment and environmental factors. The
effects of environmental parameters on the shell growth were
investigated in detail using regression analysis on the mean
increment widths as a dependent variable and environmental
factors such as seawater temperature, salinity, rainfall and tidal
change as independent variables. This method was based on
correlation, but allowed some advanced statistical analysis to
find the interrelationship between independent variables. The
two factorial ANOVA was used to analyse significant
differences between treatment levels in laboratory experiment.
3. Results
3.1 Microgrowth pattern periodicity
The mean total number of microgrowth bands deposited in
the shell layer was almost the same as the total number of
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M.-R. Mirzaei and A.T. Shau Hwai
Figure 3. Shell microgrowth pattern formed from 6 to 31 December 2011 for the individual (shell length: 13 mm, age: 5 month) of
Anadara granosa collected from Pinang Island, Malaysia (modified from Mirzaei et al. 2014b).
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tidal emersions (Figure 3). In the entire semi-monthly
periods from December 2011 to January 2012, there was
no significant different at p . 0.01 between the observed
microgrowth lines and number of tidal emersion for shells
in the intertidal area (Table 1).
3.2 Shell increment width measurement
The mean shell increment widths showed frequent high
fluctuations between 32.20 ^ 2.21 and 65.08 ^ 3.01 mm
from December 2011 to March 2012. The mean shell
increment widths remained relatively stable with very
little change from 53.23 ^ 2.05 to 59.16 ^ 3.57 mm from
April 2012 to early July 2012. It decreased slightly from
59.16 ^ 3.57 mm (July 2012) and remained at the lowest
level, which was from 25.31 ^ 2.86 to 55.09 ^ 2.18 mm
until late September 2012. Mean shell increment widths
became thicker when they achieved a width of around
58.76 ^ 3.21 to 61.06 ^ 2.13 mm over the last two
months of the study duration (Figure 4).
3.3 Environmental factors
Daily variations in the seawater temperature ranged from a
maximum of 338C to a minimum of 228C during the study
period. Figure 5 shows the frequent high fluctuations of
seawater temperature during December 2011 and January
2012. Seawater temperature was almost constant, with
slight variations from 28 to 338C during late January 2012
to late June 2012. It slowly declined from early July 2012
(28.58C) and remained at its lowest point, which varied
from 22 to 278C. Subsequently, seawater temperature
increased slightly to 308C in late September 2012. During
the last two months, the temperature remained relatively
stable from 28 to 338C.
Seawater salinity was almost constant in the range
from salinity of 29 to 31 during the one-year study period.
Three frequent high fluctuations of seawater salinity were
observed in December 2011, from April 2012 to late May
2012 and from late September 2012 to late November
2012. Seawater salinity dropped sharply and reached to the
lowest point (11 ppt) on 12 December 2011. The second
Table 1. Observed and expected numbers of growth bands in the shells of Anadara granosa kept in intertidal area from December 2011
to the end of January 2012.
Excepted no. of bands
assuming the following
periodicity
Sampling date No. of shells examined
15 Dec 2011
30 Dec 2011
14 Jan 2012
31Jan 2012
25
25
25
25
Observed mean total no. of bands
(^SD)
Daily Tidal Emersion
8.2 ^ 1.81
37.53 ^ 2.18
51.90 ^ 3.04
76.33 ^ 3.06
15
31
45
62
29
60
87
119
9
39
54
78
p Value
Daily
Tidal
þ
p , 0.01
p , 0.01þ
p , 0.01þ
p , 0.01þ
Emersion
þ
p , 0.01
p , 0.01þ
p , 0.01þ
p , 0.01þ
Note: *No significant difference from an emersion periodicity p . 0.01; þsignificant difference from tidal and daily periodicity p , 0.01.
0.0824*
0.0163*
0.0230*
0.0267*
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Figure 4.
Mean shell increment widths of Anadara granosa from Penang Island, Malaysia (December 2011– November 2012).
5
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M.-R. Mirzaei and A.T. Shau Hwai
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Figure 5.
Annual pattern of daily seawater temperature from December 2011 to November 2012 in Penang Island, Malaysia.
lowest seawater salinity was 14 ppt on 6 March 2012 and
27 October 2012 (Figure 6).
A mixed semidiurnal pattern of the tidal cycle was
observed in Penang Island, Malaysia. Tidal fluctuations of
between þ 0.1 and þ 3.0 m were recorded during the
spring tides, and þ 1.1 to þ 1.9 m during the neap tides.
Due to the cage location at the study site (þ 1.0 m), the
samples were exposed during all low tides (Figure 7).
A total of 147 rainy days were observed throughout the
study period. The highest average rainfalls were 328 and
336 mm in September and October 2012, respectively.
However, the lowest average rainfall was in January and
February 2012 at 65 and 69 mm, respectively (Figure 8).
3.4
Correlation analysis
The correlation between the environmental factors (IVs)
and mean shell increment width (DV) are shown in
Table 2. The correlation coefficient was used to determine
the correlation between the two variables. Based on
Pallant (2004) and Tabassi et al. (2012), when correlation
values were greater than 0.7, the scales were considered to
Figure 6.
have a high degree of reliability. The correlation matrix
showed that there was a strong positive correlation
between mean shell increment width and seawater
temperature (þ 0.72) and a positive correlation between
mean increment width and salinity (þ 0.53). Furthermore,
there was a very weak negative correlation between mean
increment width and rainfall (– 0.469), while there was no
correlation between mean shell growth increments and
tidal change (þ 0.071).
3.5
Multiple regression analysis
Multiple regression analysis was used to predict a
continuous dependent variable (increment width) on the
basis of several independent variables (environmental
factors). The study model was designed to find up how
much of the variance in the shell growth was explained by
the model which includes the variables of temperature,
salinity, rainfall and tidal change.
Table 3 shows the strength of the relationship between
the combination of environmental factors and mean shell
increment width. Multiple correlation coefficient between
Annual pattern of daily seawater salinity from December 2011 to November 2012 in Penang Island, Malaysia.
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Figure 7.
Annual pattern of daily tidal change between December 2011 and November 2012 in Penang Island, Malaysia.
all environmental factors and mean increment width
(R-value) was 0.780 which was highly acceptable in the
current study. The R 2 showed 60.8% of the variance in
shell increment width (DV) could be explained by
environmental variables (IVs). This was an overall
measure of the strength of association and did not reflect
the extent to which any particular environmental
parameter was associated with the increment width.
In order to evaluate the significance of the model summary,
it is essential to check the ANOVA table from the output of
multiple regression analysis. The ANOVA table indicated
that the research model was significant (F
(4,703) ¼ 273.03, P , 0.001) (Table 4).
Subsequently, coefficient table values were used to
establish how well each environmental factor (IVs) in the
research model contributed to the prediction of the
increment width (dependent variable) (Table 5). It worth
mentioning that beta values represented the unique
contribution of each environmental factor, when the
overlapping effects of all other variables were statistically
removed. As standardised coefficients converted all
environmental parameters to the same scale by SPSS
equations, the beta value was used to compare the different
Figure 8.
7
environmental variables. Temperature was the maximum
beta coefficient (0.617) and, as a result, made the greatest
unique contribution to shell growth. The lower beta value
(0.346) for salinity showed that it was the second factor
affecting shell growth (increment width). The results of
the Sig. column showed that temperature and salinity were
statistically significant in terms of their contribution to
shell growth ( p , 0.01), while tidal change and rainfall
did not contribute significantly to shell growth ( p . 0.01).
3.6 Laboratory experiment
Two-way ANOVA test showed that temperature
( p , 0.01) and salinity ( p , 0.01) significantly influence
on the increment width of Anadara granosa. After 30 days
of exposure to experimental conditions, the mean increment
widths of individuals in 31 ppt and 308C were significantly
higher than mean increment width at the other temperature
and salinity combinations, while, individuals in salinity of
26 ppt at 258C showed a mean increment width significantly
below other groups (Figure 9). Therefore, trends of these
interactive effects were an increase of shell increment with
increasing temperatures (optimum at 308C), and at high
Average monthly rainfall between December 2011 and November 2012 in Penang Island, Malaysia.
8
M.-R. Mirzaei and A.T. Shau Hwai
Table 2. Correlation matrix between mean shell increment width of Anadara granosa and each environment factor from December
2011 to November 2012.
Parameters
Increment width
Tidal change
Salinity
Rainfall
Temperature
1
0.071
1
0.530
0.071
1
2 0.46
0.024
2 0.828
1
0.72
0.09
0.35
–0.36
1
.
0.030
.
0.000
0.030
.
0.000
0.259
0.000
.
Pearson correlation
Increment width
Tidal change
Salinity
Rain fall
Temperature
Sig. (1-tailed)
Increment width
Tidal change
Salinity
Rain fall
Temperature
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(31 ppt) salinity. A scatter diagram was used to determine
the relationship between mean shell increment width and
two environmental parameters. The mean increment width
measurement showed that maximum shell growth was at
308C. However, mean increment width slowly decreased at
seawater temperatures higher than 308C (Figure 10), while
maximum shell growth was at salinity of 31 ppt (Figure 11).
4. Discussion
Cockle shell growth is a function of multiple environmental factors. It is affected by several parameters such as
food supply, temperature, population density, tidal change,
pH and water depth. In terms of the effect of
environmental factors on shell growth, there may be
some synergistic interaction between environmental
parameters such as temperature, rainfall and salinity.
Along with environment factors, endogenous aspects also
influence shell growth. While it is difficult to estimate the
actual influence of a single environmental factor on the
shell growth of cockles, multiple regression statistical
analysis can show reliable relationships between the shell
growth (dependent variable) and environmental factors
(independent variables).
In order to assess the environmental impact on shell
microgrowth increment, a year-long microgrowth increments pattern was compared with environmental records.
In order to examine the annual pattern, the following
conditions needs to be considered. First, the periodicity
rhythm of shell increment should not change during the
Table 3. Model summarya for environmental factors (IVs) and
mean increment width (DV) in the research model.
Model
1
a
b
R
R2
0.780b 0.608
Adjusted R 2 Std. error of the estimate
0.606
4.013
Dependent variable: increment width.
Predictors: (constant), temperature, tidal change, salinity and rainfall.
0.000
0.006
0.000
0.000
.
study period. Second, the shells must show continuous
growth throughout the study without cessation of growth
in different environmental conditions.
In this study, the findings indicated the precise timing
of growth line and growth increment formation in
intertidal zone. It was found that the microgrowth lines
in shell sections of Anadara granosa in intertidal zone
consist of uniform microgrowth lines. It seems possible
that these results are due to a mixed semidiurnal pattern of
the tidal cycle in Penang Island. Therefore, cockles
produced two microgrowth bands when they were emersed
twice a day (24 h). This finding is in agreement with
Richardson’s (1989) and Mahé et al.’s (2010) findings
which showed that shell microgrowth patterns in intertidal
zone mainly reflected tidal periodicity.
Analysis of environmental parameters showed that the
daily seawater temperature was fairly constant at around
30 – 338C during the study period. However, the
seawater temperature had slightly decreased to a low
range of 22 –278C from July 2012 to late September 2012.
Seawater salinity was almost constant in the range of 29–
31 ppt, except for three frequent high fluctuations in the
range of 11– 31 ppt during December 2011, April 2012 to
late May 2012 and late September 2012 to late November
2012. Rainfall investigation showed that the highest
average rainfall was 328 and 336 mm in September 2012
and October 2012, respectively, while the lowest average
rainfall was in January 2012 and February 2012 with a
total of 65 and 69 mm, respectively. Tidal change
examination showed a mixed semidiurnal pattern of the
tidal cycle in Penang Island, Malaysia.
Shell examination showed that increment width
remained relatively stable from 53.23 ^ 2.05 to
65.08 ^ 3.01 mm during the study period. Increment
widths decreased slightly in July 2012 and remained at the
lowest level which varied from 25.31 ^ 2.86 to
55.09 ^ 2.18 mm until late September 2012.
Regarding the multiple regression analysis, it was
found that temperature was the main factor affecting shell
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Table 4.
Model
1
a
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b
Regression
Residual
Total
9
ANOVAa test to assess research model.
Sum of squares
df
Mean square
F
Sig.
17594.64
11325.44
28920.09
4
703
707
4398.66
16.11
273.036
0.00b
Dependent variable: increment width.
Predictors: (constant), temperature, tidal change, salinity, rain fall.
growth (Beta value: 0.61). In addition, correlation matrix
analysis showed the shell increment width was strongly
and positively correlated to seawater temperature (0.72
coefficients out of 1). The results of this study showed that
the maximum increment width (65.08 ^ 3.01 mm) was at
the optimum temperature (308C), while continuous,
narrow increment widths from 25.31 ^ 2.86 to
55.09 ^ 2.18 mm were recorded during the lowest
seawater temperatures (22 – 278C). Therefore, lower shell
growth corresponded to lower water temperature. Nevertheless, the distance between growth bands (increment
widths) did not increase at temperatures above 308C and in
fact began to decline.
The results of this study were consistent with those of
Gosling (2008) who found that shell growth increased in a
linear manner until optimum temperature was achieved,
after which the growth rate decreased rapidly. Hiebenthal
et al. (2011) reported that high seawater temperature
increased phytoplankton concentration, thus increasing the
increment width in mollusc shells. Moreover, Page and
Hubbard (1987) found a relationship between seawater
temperature and the increment width of molluscs due to
the effects of food availability on shell increment width.
A scatter plot between temperature and increment
width showed that temperature was an important growth
regulator between 25 and 308C. However, shell growth
rate decreased sharply at temperatures above 308C.
A possible reason for the shell growth reduction above
the optimum temperature was a decrease in feeding
activity, leading to a decline in food availability, thus
leading to a breakdown in the mechanism of metabolic
activity. Isono et al. (1998) confirmed that high seawater
temperatures (. 308C) affected respiratory activities such
as heartbeat and ciliary movement of marine organisms.
As a result, when the seawater temperature was below
308C, the shell growth (increment width) of Anadara
granosa was controlled by seawater temperature because
feeding and other metabolic activities increased. Moreover, there was a similarity between optimum temperatures expressed in this study and those described by Broom
(1985) who had stated that the optimum seawater
temperature for oxygen consumption of Anadara granosa
ranged from 28 to 308C; however, when the seawater
temperature was above 308C, shell growth (increment
width) was affected by other factors. Due to the interaction
between temperature and salinity, it is essential to consider
salinity as an affective parameter during non-optimal
temperatures in the study site.
Based on Multiple regression analysis and the
correlation between environmental factors and increment
widths, salinity was the second factor affecting cockle
shell growth. Salinity fluctuations at Balik Pulau showed a
constant trend except during the heavy rainfalls of the
intermonsoon period when it was lower than other times of
the year, leading to shell valves staying closed for long
periods due to the exposure to low salinity. Consequently,
reduced the time available for feeding activity and
changed the normal metabolic rate, which later become the
main reason for lower growth rates. As a result, thinner
increments were deposited during low periods of low
salinity, as well as heavy rainfall.
The present findings seem to be consistent with other
studies which had been reported that when salinity
dropped from 31 to 10 ppt, there was severe physiological
damage to the molluscs (Kim et al. 2001). Moreover,
Hamer et al. (2008) found that cockles respond to low
salinity by closing their valves tightly when salinity is low.
In addition, these findings concur with Riisgård et al.
Table 5. Coefficienta table for the variables contributes in research model one.
Unstandardised coefficients
Model
Tidal change
Salinity
Rain fall
Temperature
a
B
Std. Error
Standardised coefficients
Beta
t
Sig.
20.14
0.94
0.03
2.06
0.25
0.11
0.03
0.08
2 0.01
0.34
0.04
0.61
2 0.56
8.07
1.03
24.09
0.57
0.00
0.30
0.00
Dependent variable: increment width.
10
M.-R. Mirzaei and A.T. Shau Hwai
Historical Biology
Figure 9.
Shell increment rate of all individuals in the laboratory experiment at temperature and salinity combinations.
(2012) who studied the seasonal changes in increment
width in cockle shells. They had indicated that a decline in
seawater salinity created a sudden reduction in the growth
of cockle shells.
These results can be compared to those of Pathansali
(1966) who stated that seawater salinity changes in Penang
Island were minimal during the dry season. However,
seawater salinity during the rainy season had a maximum
oscillation. In addition, Pathansali (1966) made a study of
the salinity requirements and preferences of Anadara
granosa in a laboratory where the feeding rates of Anadara
granosa under different salinity levels were studied. The
feeding rate was reduced by 85% at a salinity of 17.6 ppt
and was nil at 12 ppt. The findings indicated that the shell
valves were closed at very low seawater dilutions. It was
reported that Anadara granosa was able to function
relatively at salinity above 23 ppt although young specimens seemed to be able to continue their normal feeding
activity at lower salinity levels compared to older
specimens.
This study concerning Anadara granosa shell growth
provides new insights for the understanding of growth
patterns in Penang Islands, west coast of Malaysia. The
sclerochronological approach appears as a powerful tool to
characterise high-frequency variations in the shell growth
in relation to environmental parameters. This approach
allowed us to prospective analysis of culture location and
environmental assessment of farm related to tidal levels.
The results of this investigation show that analysis of
increment width in the shell cross section of Anadara
granosa leads to an accurate estimation of the environmental effects during their life history. One of the most
significant findings to emerge from this study is that cockle
shell growth was mainly controlled by temperature and
less by salinity, while rainfall and tidal changes were
insignificant. The second major finding is that the growth
rate of Anadara granosa was in a linear trend to optimum
temperature, while salinity contributes to shell growth as a
moderator at temperatures above the optimum. In addition,
Anadara granosa responded to variations in seawater
salinity by closing its shell valves and changing its feeding
activity and normal metabolism. This study shows that
shell microgrowth increments were well defined and
deposited with a tidal periodicity in the intertidal zone,
providing the calendar base for high-resolution ecological
studies and environmental reconstruction from shell
cockles Anadara granosa.
Figure 10. Scatter plot of the shell increment rate of all
individuals in the laboratory experiment versus different water
temperatures.
Figure 11. Scatter plot of the shell increment rate of all
individuals in the laboratory experiment versus different
seawater salinity.
Historical Biology
Acknowledgements
The authors would like to acknowledge the Marine Science
Laboratory, School of Biological Sciences, Universiti Sains
Malaysia, for their support and contribution to this study.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Historical Biology
References
Brock V, Bourget E. 1989. Analyses of shell increment and microgrowth
band formation to establish seasonality of mesolithic shellfish
collection. J Dan Archaeol. 8(1):7–12.
Broom M. 1985. The biology & culture of marine bivalve molluscs of the
genus Anadara. Manila: WorldFish Center.
Cerrato RM, Wallace HV, Lightfoot KG. 1991. Tidal and seasonal
patterns in the chondrophore of the soft-shell clam Mya arenaria.
Biol Bull. 181(2):307–311.
Epplé VM, Brey T, Witbaard R, Kuhnert H, Pätzold J. 2006.
Sclerochronological records of Arctica islandica from the inner
German Bight. Holocene. 16(5):763–769.
Gibson R, Barnes M, Atkinson R. 2001. Molluscs as archives of
environmental change. Oceanogr Mar Biol Annu Rev. 39(1):103–164.
Gillikin DP, Lorrain A, Navez J, Taylor JW, André L, Keppens E,
Baeyens W, Dehairs F. 2005. Strong biological controls on Sr/Ca
ratios in aragonitic marine bivalve shells. Geochem Geophys
Geosyst. 6(5):1–16.
Goodwin DH, Flessa KW, Schöne BR, Dettman DL. 2001. Crosscalibration of daily growth increments, stable isotope variation, and
temperature in the Gulf of California bivalve mollusk Chione cortezi:
implications for paleoenvironmental analysis. Palaios. 16(4):
387 –398.
Gosling E. 2008. Bivalve molluscs: biology, ecology and culture. Oxford:
Wiley-Blackwell.
Hamer B, Jakšić Ž, Pavičić-Hamer D, Perić L, Medaković D, Ivanković
D, Pavičić J, Zilberberg C, Schröder HC, Müller WE. 2008. Effect of
hypoosmotic stress by low salinity acclimation of Mediterranean
mussels Mytilus galloprovincialis on biological parameters used for
pollution assessment. Aquat Toxicol. 89(3):137–151.
Hiebenthal C, Philipp E, Eisenhauer A, Wahl M. 2011. Interactive effects
of temperature and salinity on shell formation and general condition
in Baltic Sea Mytilus edulis and Arctica islandica. Aquat Biol. 14(3):
289 –298.
Isono R, Kita J, Kishida C. 1998. Upper temperature effect on rates of
growth and oxygen consumption of the Japanese littleneck clam,
Ruditapes philippinarum. Bull Jpn Soc Sci Fish. 64(3):373–376.
Kim W, Huh H, Huh S-H, Lee T. 2001. Effects of salinity on endogenous
rhythm of the Manila clam, Ruditapes philippinarum (Bivalvia:
Veneridae). Mar Biol. 138(1):157–162.
Kozminsky E, Lezin P. 2007. Distribution of pigments in the shell of the
gastropod Littorina obtusata (Linnaeus, 1758). Russ J Mar Biol.
33(4):238–244.
Mahé K, Bellamy E, Lartaud F, De Rafelis M. 2010. Calcein and
manganese experiments for marking the shell of the common cockle
(Cerastoderma edule): tidal rhythm validation of increments
formation. Aquat Living Resour. 23(03):239–245.
Marchitto Jr TM, Jones GA, Goodfriend GA, Weidman CR. 2000. Precise
temporal correlation of Holocene mollusk shells using sclerochronology. Quat Res. 53(2):236–246.
Matozzo V, Marin M. 2011. Bivalve immune responses and climate
changes: is there a relationship? Invert Surviv J. 8(1):71–77.
View publication stats
11
Mirzaei MR, Yasin Z, Hwai ATS. 2014a. Length-weight relationship,
growth and mortality of Anadara granosa in Penang Island,
Malaysia: an approach using length-frequency data sets. J Mar Biol
Assoc UK FirstView. 95(2):381–390.
Mirzaei MR, Yasin Z, Hwai ATS. 2014b. Periodicity and shell
microgrowth pattern formation in intertidal and subtidal areas
using shell cross sections of the blood cockle, Anadara granosa.
Egypt J Aquat Res. 40(4):459–468.
Mubiana VK, Blust R. 2007. Effects of temperature on scope for growth
and accumulation of Cd, Co, Cu and Pb by the marine bivalve
Mytilus edulis. Mar Environ Res. 63(3):219–235.
Neves RJ, Moyer SN. 1988. Evaluation of techniques for age
determination of freshwater mussels (Unionidae). Am Malacol
Bull. 6(2):179–188.
Page H, Hubbard D. 1987. Temporal and spatial patterns of growth in
mussels Mytilus edulis on an offshore platform: relationships to
water temperature and food availability. J Exp Mar Biol Ecol. 111(2):
159– 179.
Pallant J. 2004. SPSS survival manual: a step by step guide to data
analysis using SPSS (version 15). Maidenhead: Open University
Press.
Pathansali D. 1966. Notes on the biology of the cockle, Anadara granosa
L. Proc Indo-Pacific Fish Counc. 11(2):84–98.
Riascos J, Guzman N, Laudien J, Heilmayer O, Oliva M. 2007. Suitability
of three stains to mark shells of Concholepas concholepas
(Gastropoda) and Mesodesma donacium (Bivalvia). J Shellfish Res.
26(1):43– 49.
Richardson C. 1987. Microgrowth patterns in the shell of the Malaysian
cockle Anadara granosa (L.) and their use in age determination.
J Exp Mar Biol Ecol. 111(1):77–98.
Richardson C. 1989. An analysis of the microgrowth bands in the shell of
the common mussel Mytilus edulis. J Mar Biol Assoc UK. 69(02):
477– 491.
Richardson C, Crisp D, Runham N, Gruffydd L. 1980. The use of tidal
growth bands in the shell of Cerastoderma edule to measure seasonal
growth rates under cool temperate and sub-arctic conditions. J Mar
Biol Assoc UK. 60(04):977–989.
Riisgård HU, Bøttiger L, Pleissner D. 2012. Effect of salinity on growth
of mussels, Mytilus edulis, with special reference to Great Belt
(Denmark). Open J Mar Sci. 2(4):167–176.
Sato S. 1999. Temporal change of life-history traits in fossil bivalves: an
example of Phacosoma japonicum from the Pleistocene of Japan.
Palaeogeogr Palaeoclimatol Palaeoecol. 154(4):313– 323.
Schöne BR, Oschmann W, Rössler J, Castro ADF, Houk SD, Kröncke I,
Dreyer W, Janssen R, Rumohr H, Dunca E. 2003. North Atlantic
Oscillation dynamics recorded in shells of a long-lived bivalve
mollusk. Geology. 31(12):1037–1040.
Schöne BR, Rodland DL, Surge DM, Fiebig J, Gillikin DP, Baier SM,
Goewert A. 2006. Comment on ‘Stable carbon isotopes in freshwater
mussel shells: environmental record or marker for metabolic
activity?’ by J. Geist et al.(2005). Geochim Cosmochim Acta.
70(10):2658 –2661.
Selin N. 2000. Shell form and growth of the bivalve Scapharca
broughtoni. Russ J Mar Biol. 26(3):204–208.
Simpson JH, Sharples J. 2012. 2012 Introduction to the physical and
biological oceanography of shelf seas. Cambridge, UK: Cambridge
University Press.
Tabassi AA, Ramli M, Bakar AHA. 2012. Effects of training and
motivation practices on teamwork improvement and task efficiency:
the case of construction firms. Int J Proj Manag. 30(2):213–224.
Wanink JH, Zwarts L. 1993. Environmental effects of the growth rate of
intertidal invertebrates and some implications for foraging waders.
Neth J Sea Res. 31(4):407–418.
Yaroslavtseva L, Sergeeva E. 2006. Adaptivity of the bivalve Mytilus
trossulus larvae to short-and long-term changes in water temperature
and salinity. Russ J Mar Biol. 32(2):82–87.