ICES Journal of Marine Science, 61: 1253e1259 (2004)
doi:10.1016/j.icesjms.2004.07.025
Age and individual growth of Mesodesma mactroides (Bivalvia)
in the southernmost range of its distribution
Sandra M. Fiori and Enrique M. Morsán
Fiori, S. M., and Morsán, E. M. 2003. Age and individual growth of Mesodesma mactroides
(Bivalvia) in the southernmost range of its distribution. e ICES Journal of Marine Science,
61: 1253e1259.
The yellow clam, Mesodesma mactroides, is an intertidal bivalve typical from sandy
beaches of the South American Atlantic coast. Growth parameters of southernmost
populations of M. mactroides were studied and compared with other populations. Thin shell
sections were examined to describe internal shell layers and to contrast with external shell
transparency. Periodicity of deposition of external growth increments was studied recording
the degree of transparency of the shell border. Growth patterns were determined using
modal progression analysis from size frequency distributions, analysis of external shell
increments, and size-at-age data derived from inner shell layers. Growth parameters were
described using the von Bertalanffy growth model. Both internal and external patterns were
coincident and exhibited a succession of one translucent and one opaque region. The
transparent region was deposited during summer. Growth differences found between
populations may be related to unequal size of first ring in both beaches. This feature may
originate from asynchrony in spawning and recruitment. The monthly analysis of shell
length size frequency distribution shows that growth of M. mactroides is seasonal.
Estimations of asymptotic size of studied populations and others located at the southern
(coldest) half of the geographical range of distribution suggest a negative relation with
latitude.
Ó 2004 Published by Elsevier Ltd on behalf of International Council for the Exploration of the Sea.
Keywords: bivalves, growth parameters, surf clam, yellow clam.
Received 30 September 2003; accepted 30 July 2004.
S. M. Fiori: Departamento de Biologı́a, Bioquı́mica y Farmacia, Universidad Nacional del
Sur, San Juan 670, Bahı́a Blanca (8000), Argentina. E. M. Morsán: Instituto de Biologı́a
Marina y Pesquera Alte. Storni, Costanera S/N, San Antonio Oeste (8520), Argentina.
Correspondence to S. Fiori: tel: C54 291 4595100; fax: C54 291 4595130; e-mail:
sfi[email protected].
Introduction
The yellow clam, Mesodesma mactroides (Deshayes 1854),
is an intertidal bivalve characteristic from sandy beaches of
the South American Atlantic coast. Its distribution ranges
from Brazil (24(S) to Argentina (41(S). This range
includes hundreds of kilometres in Brazil, 22 km in
Uruguay, and 375 km of beaches in Argentina (Olivier
and Penchaszadeh, 1968) (Figure 1).
A progressive and so far unexplained mass mortality
affected most of the known populations of this species from
Brazil to Argentina between 1993 and 1995 (Méndez, 1995;
Odebrecht et al., 1995; Fiori, 1996). After these events, the
southernmost populations in the species’ natural range,
located at Monte Hermoso (38(59#S 61(15#W) and Isla
del Jabalı́ (40(33#S 62(14#W) (Figure 1) became relevant
for two reasons: (i) the populations at Monte Hermoso was
almost decimated in about ten days in November 1995 (the
number of dead individuals was estimated at about 63
1054-3139/$30.00
million) (Fiori and Cazzaniga, 1999); (ii) the population at
Isla del Jabalı́ was the only one that escaped the mass
mortality phenomena.
We began to study the population dynamics of yellow
clam at Monte Hermoso, before mass mortality and at Isla
del Jabalı́ in 1998 (Fiori, 2002; Fiori et al., 2004). In this
paper we aim to estimate the growth parameters (a previous
requisite for the development of population models) of the
southernmost populations of Mesodesma mactroides and
compare them with parameters of other populations.
Ageing methods traditionally used in bivalves include
examination of external valve surfaces for growth check
rings that are deposited in winter (Richardson and Walker,
1991). In many species, however, the rings may be absent
or difficult to discriminate, as in the case of the first year
growth marks and the closely packed rings laid down later
in the life of the specimen (Richardson et al., 1993). An
alternative method to estimate age is the study of the optical
pattern of internal bands in shell cross-sections or in acetate
Ó 2004 Published by Elsevier Ltd on behalf of International Council for the Exploration of the Sea.
1254
S. M. Fiori and E. M. Morsán
0
Blanca
Bay
10
20
30 km
45º
39º
Monte
Hermoso
63º
57º
51º
24º
Brazil
28º
Anegada
Bay
32º
Uruguay
Uy
36º Argentina
Isla del
Jabalí
NA
Atlantic
Ocean
40º
Figure 1. Geographic distribution of Mesodesma mactroides
(adapted from Olivier et al., 1971), and a map of the south of
Buenos Aires province showing the study areas (Monte Hermoso
and Isla del Jabalı́) and names of other populations cited in the text
(NA: northern of Argentina, Uy: Uruguay).
peels. The less common method of preparation of bivalve
shells is by thin sectioning. Even though more laborintensive, thin sections tend to produce superior results than
acetate peels (Cerrato, 2000). The internal growth bands are
more clearly defined and easier to count in shell structures
such as hinge plates and chondrophores (Thompson et al.,
1980; Palacios et al., 1994). Ageing studies of yellow clam
were based on shell section (Uruguay) and external rings
(northern Argentina). Growth is generally studied by
length-based methods and by counting external growth
rings (Olivier et al., 1971; Arreguin-Sánchez et al., 1991;
Defeo et al., 1992a, b).
These studies reveal differences between stocks from
Uruguay and Argentina. The first describes fast growing
and short-lived individuals (lifespan 3.5 yr), and the growth
rate shows seasonal variation and density-dependence
(Defeo et al., 1992a, b). Olivier et al. (1971) did not report
seasonal variations in growth in clams from northern
Argentina, but estimated lower growth rate and greater
longevity (8 yr) than the studies carried out in Uruguay.
These differences may be a response to dissimilar environmental characteristics (McLachlan et al., 1996).
Material and methods
This study was carried out in Monte Hermoso and Isla del
Jabalı́, two exposed sand beaches separated by huge extensions of salt-marshes and estuaries in the southern coast of the
Buenos Aires province (Figure 1). Both beaches have
a smooth slope, fine sand, and are backed by a fringe of
dunes. The tide levels vary from 1 to 3 m. The mean annual
water temperature is approximately 14(C, with a mean
maximum temperature of 22(C and mean minimum near
7(C (Fiori, 2002).
Samples from Monte Hermoso were taken during May
and November 1995. The first set consisted of nonquantitative and non-selective samples taken at several
points along the beach, digging in the sand. The second set
was taken during the mass mortality episode described in
Fiori and Cazzaniga (1999). For ageing studies, a subsample
of 142 clams of all sizes was used (104 clams from the first
sampling and 40 from the second).
Samples of Isla del Jabalı́ were obtained in an intertidal
fringe in two different ways. (i) Systematic surveys (August
1998 and March 2000): samples were taken at 4-m intervals
along six transects located perpendicular to the coastline.
Distance between transects was 2 km. (ii) Periodic sampling
( from September 1998 to October 1999): stratified random
sampling was carried out at two sites, 4 km apart. In each
sampling, the intertidal zone was divided into 20-m width
strata parallel to the coastline. Six quadrats were randomly
placed within each strata. A subsample of 85 clams was
taken to the laboratory for ageing studies (56 clams from
systematic surveys and 26 clams from periodic sampling)
and a fraction of the sample was separated to analyse the
shell marginal borders monthly in order to validate ageing.
In both beaches, clams and sediment were removed and
sieved at 1 mm in order to retain the juveniles. Clams were
counted and measured at 0.1 mm precision.
Age was determined using thin shell sections in which the
optic pattern of internal growth bands was crosschecked
with the external bands. The thin sections were obtained by
cutting the valve with a low-speed diamond saw from the
umbo to the ventral margin, through the ligament platform.
This internal section of the valve was ground and polished
using sandpaper of very fine grain (4000 grit) on a polishing
machine. The polished surface was mounted on a microscope slide. A thin section of 0.3e0.4 mm was obtained
with a second cut. The thin section was ground and polished
again with sandpaper (4000 grit), until adequate thickness
and texture were reached. The preparation was observed
under a dissecting microscope with transmitted light to
establish the optical pattern of inner shell layers for further
comparison with the external growth marks.
Periodicity of deposition of external growth increments
was studied by recording the degree of transparency of the
border ring in monthly samples.
Growth patterns were determined using three different
techniques: modal progression analysis from size frequency
distributions (SFD), analysis of external shell increments,
and size-at-age data derived from inner shell layers.
Individual cohorts were identified from SFD by modal
progression analysis using the Bhattacharya method (FISAT
software), and ages were assigned by cross-checking with
Age and individual growth of Mesodesma mactroides
growth ring data. Growth increments recorded on shell
external surface were measured from the umbo to the
beginning of the transparent band.
Due to the summer spawning, the date selected to serve
as the reference for ageing was 1 January (the austral
summer).
Growth parameters were described using von Bertalanffy
growth model for all three data sets,
ÿ
Lt ZLN 1 ekðtt0 Þ
where LN is the asymptotic size (in mm), k the constant of
annual growth, t the age ( years), and t0 is the age at size zero.
A seasonal form of the von Bertalanffy model (Hoenig
and Hanumara, 1982; Sommers, 1988) was also fitted to
SFD data of Isla del Jabalı́:
ÿ
Lt ZLN 1 e½kðtt0 ÞT1 T2 T1 Z½C sinð2pðt ts ÞÞ=2p
T2 Z½C sinð2pðt0 ts ÞÞ=2p
1255
where C Z parameter reflecting the intensity of seasonal
growth oscillation, and ts Z starting time of sinusoid
growth oscillation.
Growth models were fitted to data using maximum likelihood and compared using likelihood ratio test, in order to
evaluate the following sources of growth variability: (i)
Variability of first ring size between cohorts was tested by
single ANOVA. A posteriori Scheffé contrasts were
performed to test variability between populations. (ii) Differences in growth parameters between Isla del Jabalı́ and
Monte Hermoso populations from external growth marks
and inner shell layer data. Parameters were compared by
likelihood ratio test (Kimura, 1980; Cerrato, 1990). This
method allows the testing of several hypotheses to compare
two curves by analysing one or more growth parameters
simultaneously. (iii) Seasonal variability was analysed
using modal progressions from SFD. Seasonal parameters
of growth models were tested through likelihood techniques. Contrast between traditional and seasonal models was
performed by testing the single null hypothesis, C Z 0,
with likelihood ratio test.
Growth data estimated in this study were compared with
data available from the literature on M. mactroides at lower
latitude.
Region
opaque
Region
translucent
A
Cut plane
Microincrement
B
Annual cycle
Figure 2. (A) Shell of yellow clam showing on the external surface a pattern composed by a succession of translucent and opaque regions,
and in the internal surface the plane of cutting. (B) Thin sections of condrophore showing an annual growth cycle pattern and
microincrements (sub-annual growth lines).
S. M. Fiori and E. M. Morsán
Results
1.0
0.8
Proportion
80
70
0.6
0.4
0.2
60
50
40
30
20
10
0
0
1
2
3
4
5
6
7
8
5
6
7
8
Age (years)
External annual increments (mm)
Figure 2A shows the shell external and internal surfaces
of a yellow clam. The external surface exhibited an
annual growth cycle pattern composed by a succession of
translucent and opaque regions. Analysis of the transparency of the shell border allowed validation of the
annual formation of each combination (Figure 3). The
seasonal cycle in the internal shell layers observed in
thin sections and external increments showed coincident
patterns. These consist of a broad translucent region
formed during summer, and a thin opaque region deposited
from fall to late spring. The first band is translucent and the
transition between regions is gradual. This is due to a condition of intermediate shell transparency in autumn and
spring (Figure 2B).
Additional information was obtained from thin sections
ground to a thickness 100 mm. These sections show 21e25
narrow translucent bands within the annual growth cycle
pattern. The bands are closely deposited in the opaque
region, but more separated in the translucent region (Figure
2B), and seem to be related to the fortnightly cycle of high
tides.
Three year classes were identified from the Isla del Jabalı́
population: 1998, 1997, and 1996. In the same way, year
classes identified from Monte Hermoso population were
1993, 1994, and a joint one composed of 1991 and 1992.
Size of the first ring (measured until the end of opaque
band) shows highly significant differences between all
cohorts (ANOVA test, p ! 0.05). However, Scheffé
contrast revealed that a high percentage of such variation
(82.5%) was explained by geographic localization: the size
of the first ring of clams from Isla del Jabalı́ was
significantly greater than that from Monte Hermoso. Clam
growth is very fast during the first two years of life, and
decreases during subsequent years. During early growth,
both broad transparent and opaque bands are wide.
Maximum likelihood growth models of two populations
are showed in Figure 4 and growth parameters are
summarized in Table 1.
Models estimated from sizeeage data were not significantly different for all the hypotheses of the likelihood
ratio test (Table 2). Maximum asymptotic size showed low
probability (chi-square, p Z 0.06). This may be derived
from the range of ages present in valves analysed: the
majority of ages recorded in valves of the Monte Hermoso
population (71%) were younger than 2 years, while such
young clams of the Isla del Jabalı́ population represented
only 18% of the sample. Growth curves estimated from
external increments were significantly different under the
hypothesis of three identical parameters ( p ! 0.001).
Monthly shell length frequency distribution from Isla del
Jabalı́ is given in Figure 5, showing clear polymodality and
poor recruitment since 1998. A few small individuals were
present in samples in March and April of 1999 and 2000.
Bhattacharya analysis of changes in size of several
cohorts suggests growth differences between months.
Results of both traditional and seasonal von Bertalanffy
models are presented in Table 1. The seasonal model was
Shell Length (mm)
1256
80
70
60
50
40
30
20
10
0
0
1
2
3
4
Age (years)
J
F
M
A
M
J
J
A
S
O
Monte Hermoso
Opaque
Translucent
Figure 3. Monthly proportion of clams with the border ring of the
shell opaque or transparent during 1999 (n Z 141).
Isla del Jabalí
Figure 4. Growth models of two populations of Mesodesma
mactroides estimated from shell sizeeage data and external annual
increments length.
Age and individual growth of Mesodesma mactroides
1257
Table 1. Growth parameters estimated for several populations of Mesodesma mactroides located at different latitude [Data from (a) Defeo
et al., 1992b (b) Defeo et al., 1992a (c) Olivier et al., 1971].
SFD
Beaches
Uruguay
(a)
(b)
Northern Argentina (c)
Monte Hermoso
Isla del Jabalı́
External annual increments
Size at age
k
LN
t0
C
ts
k
LN
t0
k
LN
t0
0.82
0.64
d
83
100
d
0
0.24
d
1
d
d
0.2
d
d
d
d
d
d
d
d
d
d
d
0.90
d
0.28
75.47
d
83.76
0.04
d
1.62
d
d
d
d
d
0.48
74.66
0.23
0.54
70.42
0.36
0.49
0.47
78.42
79.13
0.44
0.45
d
0.45
d
0.09
0.59
d
72.77
d
0.43
d
0.42
d
77.73
d
0.51
d
the best fit to the data (chi-square, p ! 0.001), and curve
fitting is shown in Figure 6.
Discussion
Yellow clams are seasonal migrants that move into the
intertidal fringe during certain times of the year (Coscarón,
1959). In winter, adults are found deeper in the sediments
and below the swash zone, while in summer they are
located almost above the swash zone (upper intertidal level)
(McLachlan et al., 1996). Different seasonal water
temperature and burrowing appear to be relevant in
determining the transparency pattern of the shell. Cerrato
(2000) suggests that the transparency pattern of Mya
arenaria is affected by metabolic activity and matches
seasonal changes in bottom-water temperature. Lewis and
Cerrato (1997) studied microgrowth increments and found
that shell transparency changed quickly in response to
abrupt changes in environmental variables. Also, their
results indicated that the shell growth remained correlated
with metabolic rate, even when somatic and shell growth
are uncoupled. They proposed that the deposition of
translucent, thin increments was caused by a high metabolic
rate and a short immersion period. A moderate metabolic
rate during an extensive period of immersion could produce
a wide opaque increment.
In M. mactroides the transparent region is deposited
during summer, when they live close to the sand surface,
exposed during low tide and influenced by high air
temperature. If the deposition pattern proposed for
M. arenaria is correct for M. mactroides, the degree of
shell transparency could be explained by metabolic rate and
seasonal migration, rather than reproductive activity.
However, this study has been the only one that describes
thin sectioning of shell in the yellow clam, and microgrowth analysis was beyond its scope.
Growth differences between populations may be related
to unequal size of the first ring, as described above. This
feature may have originated by asynchrony in spawning
and recruitment. Thus, at the moment of formation of
the next transparent band (during the following summer)
the individuals of year classes 0C from two populations
differ in age.
The results from the SFD in this work show that growth
of M. mactroides is seasonal. Defeo et al. (1992a) describe
seasonal growth for populations from Uruguay, and
attribute such variability to high temperature fluctuations
(14(C difference between summer and winter), and the
response of clams to these fluctuations.
Table 2. Comparison of growth parameters estimated from length-at-age and annual increment data by likelihood ratio test.
Estimation
Method
Length-at-age
Annual increment
Ho1
LNIS Z LNMH
Ho2
kIS Z kMH
Ho3
t0IS Z t0MH
Ho4
QIS Z QMH
Ho5
LNIS, kIS Z LNMH, kMH
0.067
0.677
0.226
0.303
0.651
0.314
0.244
0.000
0.126
0.177
(IS) Isla del Jabalı́, (MH) Monte Hermoso, (Q) LN, k, t0.
1258
S. M. Fiori and E. M. Morsán
80
n = 836
08/98
70
10/98
Length (mm)
60
n =1279
50
40
30
20
10
0
0
1
2
12/98
3
4
5
6
Age (years)
n =744
Figure 6. Growth seasonal model of Mesodesma mactroides from
Isla del Jabalı́ estimated from length frequency distribution data.
02/99
100
n =1049
L∞
Frequency
90
03/99
80
n = 584
70
60
33
04/99
35
n = 806
37
39
41
Latitude (º)
Figure 7. Growth parameters estimated by several populations of
Mesodesma mactroides located at different latitude.
06/99
growth rate in Uruguay (described by Defeo et al. (1992a,
b) is higher than in the southern populations (Table 2). The
effect of temperature on growth seems to affect asymptotic
size estimation. Several estimates of asymptotic size of
populations located at the southern (coldest) half of the
geographical range of distribution suggest a negative
relationship with latitude (Figure 7), but this may be better
understood if growth studies on other populations, along
with quantitative and qualitative studies of phytoplankton,
were carried out.
n = 285
03/00
0
n = 347
10
20
30
40
50
60
70
80
Shell Length (mm)
Figure 5. Monthly length frequency distribution of Mesodesma
mactroides from Isla del Jabalı́ ( from August 1998 to March 2000).
With the results obtained in this study and the literature
data on M. mactroides, it is possible to discuss the influence
of latitude-dependent environmental factors on growth and
other aspects of population dynamics, and it can be
assumed that temperature and food availability are key
factors. Temperatures decrease from north to south as does
the period for optimum growth and recruitment. Indeed,
Acknowledgement
We thank Eliana Bontti for her critical reading of the
manuscript.
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