J. MolL Stud. (1998), 64,407-421
> The Malacological Society of London 1998
MICROEVOLUTION AND PHENOTYPIC PLASTICITY IN
DONAX SERRA RODING (BIVALVIA: DONACIDAE) ON
HIGH ENERGY SANDY BEACHES
ALEXANDRE G. SOARES1, ROBERT K. CALLAHAN and A.M.C. DE RUYCK
Zoology Department and Institute for Coastal Research, University of Port Elizabeth - P.O. Box 1600,
Port Elizabeth - 6000 - South Africa
(Received 15 October 1997; accepted 5 January 1998)
ABSTRACT
Morphological differences between populations of
the wedge clam Donax serra inhabiting two different
coasts and biogeographic regions of South Africa
were investigated. Both adults and juveniles occupied different positions along the beach gradient
depending on the coast: on the southeast coast adults
occurred in the mid intertidal and juveniles and
recruits were low intertidal to subtidal; on the west
coast the zonation pattern was reversed. Not only
adults but also juvenile clams had shapes differing
significantly between the two coasts; west coast clams
were thinner, rounder and had a higher body density
than the southeast ones—recruits were less dense in
the former coast. Differences in shell shape between
coasts are probably the result of directional selection
on the adults with the microevolutionary changes
being maintained by geographical isolation. Shell
density, on the other hand, seems to be environmentally determined through physiological control
of shell calcification, i.e. more mobile intertidal clams
having lower shell density than less mobile subtidal
clams. Ontogenetic changes in shape and density are
presumably adaptive and appear to be related to
mobility, i.e. the larger, heavier and denser adults
being more stable in the substrate, and the smaller,
thinner and less dense juveniles being more mobile
and dispersive. Phenotypic plasticity in present D.
serra populations is an important factor that enabled
this species to occupy different habitats and biogeographic regions and to survive 5 million years of
environmental changes.
INTRODUCTION
Phenotypic plasticity is a common feature of
many species and is believed to be a response
of individuals to changes in the physical (Grant,
1991) and/or biological environment (Levitan,
1
Present Address: Laboratory for Ecology and Aquacuiture, Zoological Institute, Kathobc Univenitdl, Leuven, Naamsestnal 59 B-3000,
Leuven, Belgium. E-mail: agtoaresdeudoranuulcom
1988). A phenotypic characteristic, however,
may be determined solely by the genetic structure, i.e. genotype, of a species or population
(Rothwell, 1993), or by the interaction between
genes and the environment (Pigliucci, 1996).
Selection pressure acting upon a diverse phenotype, which is genetically determined, will
trigger evolutionary changes while environmentally determined plasticity may buffer them
(Grant, 1991).
Bivalves of the genus Donax inhabit dynamic
environments, i.e. high energy beaches of tropical and temperate coasts (Ansell, 1983). These
clams have wedge-shaped shells which seem to
be an adaptation for migrating between tidelevels and for rapid burrowing (Stanley, 1970).
Tidal migrations aid clams to maintain a
position in the ecosystem that optimizes their
feeding rates and minimizes predation risk
(Ansell, 1983). Amongst Donax species there
is high interspecific (Stanley, 1970; Ansell
1985; McLachlan, Jaramillo, Defeo, Dugan, De
Ruyck & Coetzee, 1995) and intraspecific
(Wade, 1967; Donn, 1990a) variability in shell
shape. For populations of the same species
occurring in different biogeographic positions,
morphological variability has been associated
solely with habitat differences (Donn, 1990a)
and microevolutionary differentiation has been
neglected. In some species of large sized
Donax, such as Donax serra, clams undergo a
marked ontogenetic change in zonation (De
Villers, 1975; Prosch & McLachlan, 1984),
physiological responses (Ansell & McLachlan,
1980; Stenton-Dozey & Brown, 1994) and
shell shape (this study). Although changes in
physiological responses of D. serra have been
associated with changes in zonation (StentonDozey & Brown 1994; Soares, McLachlan &
Schlacher, 1996), the adaptive value of ontogenetic changes in morphology has not yet
been addressed for this species.
408
A.G. SOARES, R.K. CALLAHAN & M.C. DE RUYCK
The objectives of this study are threefold: i)
to verify if morphological variability between
Donax serra populations is related, not only
to habitat, but also to historical (evolutionary)
causes, ii) to describe the ontogenetic changes
in morphology and density, and discuss their
adaptive value and iii) to highlight the evolutionary importance of phenotypic plasticity in
changing environments such as sandy beaches.
METHODS
Study areas
Adults and juveniles of Donax serra Roding were
collected from beaches in two different biogeographic provinces—two beaches from the cold west
coast and two beaches from the cool southeast coast
of South Africa (Fig. 1).
The west coast is bathed by the cold waters of the
Benguela current, Atlantic Ocean. The Benguela
Current originates largely at the subtropical con-
vergence from Atlantic Central Water. It flows northwards reinforced by the cold waters of the circumAntarctic West Wind Drift (Brown & Jarman, 1978)
till 15°S where it is deflected westwards (Shannon,
1985). The Benguela region is one of the 4 major
upwelling systems of the world. During summer, cold
waters come from 100-300 m depth to the surface
at a rate of 20 m per day after strong southeast winds
(Shannon, 1985). Temperature ranges from 8 to
14°C in summer and 11 to 17°C in winter (StentonDozey & Brown, 1994) averaging 13°C annually. The
beaches sampled on this coast were Silwerstroomstrand—a modally dissipative beach with fine sands,
gentle slope and waves larger than 2 m, and Bloubergstrand, an intermediate beach with coarse sands,
a steep slope and waves of 1.5 m high (Soares et al.,
1996).
The southeast coast is bathed by the warm waters
of the Agulhas Current, Indian Ocean. The Agulhas
Current is a southflowingbranch of the South Equatorial and the Mozambique Currents. It flows parallel
to the edge of the southeastern shelf of Africa until
reaching the Agulhas Bank where it is deflected
southwestwards (Brown & Jarman, 1978). Both
18°S
24°S
30°S
Agulhas
current
27°E
33°E
Figure 1. Study beaches on the South African coast. Sw - Silwerstroomstrand, B - Bloubergstrand, S - Silver
Sands, H - Hermanus, M - Maitlands, SR - Sundays River.
MICROEVOLUTION IN DONAX SERRA
studied beaches, Maitlands in St. Francis Bay and
Sundays River in Algoa Bay, may experience cold
waters upwelled during strong summer eastern winds
(Goschen & Schumann, 1995), although much less
frequently than beaches of the west coast (Shannon,
1985). Mean annual sea temperature in this region is
22°C, ranging from 15 to 17°C in winter and reaching
a summer maximum of 26°C (Ansell & McLachlan,
1981; Stenton-Dozey & Brown, 1994). Both beaches
are in a high energy intermediate to dissipative
morphodynamic state, having fine to medium sands,
moderate slopes and waves of 1.5 m high (McLachlan, 1990).
Sampling methods
Sampling was conducted during spring low-tides
between April and July of 1996. Depending on the
beach width, 15 to 19 regularly spaced stations were
established along a transect perpendicular to the
shore line on each beach. The transects extended
from the base of the foredunes to 1 metre depth in
the surf zone. Triplicate quadrats, of 0.1 m2 each,
were dug at each station to a depth of about 30 cm
and the sediment was sieved through a 1 mm
diameter mesh bag on the southeast coast, and 2 mm
diameter mesh on the west coast. The retained clams
were preserved in 10% formalin.
A graduated staff and dumpy level were used to
measure the beach profiles. The depth of the ground
water table was also measured at each station. One
sample of sand was collected at each station for
standard particle size analysis with the binocular
microscope (Pettijohn, Potter & Siever, 1987). Eight
visual estimations of breaking wave heights and
periods were performed utilizing a measuring staff
and a stop watch, respectively (Bascom, 1964). The
wave parameters and beach grain size of each beach
were then utilized to characterize the morphodynamic state during the sampling date. This is calculated by the dimensionless fall velocity index O, also
known as Dean's parameter, using the following
equation (Wright & Short, 1984):
n=
,. T
where H b is the breaker height in cm, T is the wave
period in s and W, is the mean beach sediment fall
velocity in cm.s"' (this value was taken from tables of
sediment size X fall velocity experimentally tested by
Gibbs, Matthews & Link, (1971) using glass spheres
with the same specific density as quartz sand).
Zonation and morphometric measurements
Previous studies have found that both adult and
juvenile zonation patterns differ between west and
southeast coast D. serra populations; adults occur at
high and juveniles at low intertidal positions on the
southeast coast and vice-versa on the west coast. (De
Villiers, 1975; Prosch & McLachlan, 1984). Donn
(1990b) failed to find this contrasting adult-juvenile
zonation and concluded that only adults change
zonation between coasts. To test if both adults and
409
juveniles differ in zonation between the two coasts,
we performed a regression analysis Type I of clam
size (length) against the clam's position in the intertidal for each beach and tested for significant differences amongst slopes with the F test (Sokal & Rohlf,
1981).
For the morphometric analyses, a total of five
morphological variables were measured on each clam
from each coast. Shell length (antero-posterior),
height (ventro-dorsal) and width (left-right) of the
valves were measured to 0.01 cm with vernier callipers; wet mass—i.e. flesh and shell—was measured
to the nearest 0.01 g on a top loading balance; total
body volume, i.e. flesh and shell, was determined to
0.1 ml by measuring the volume of water displaced by
each clam in a calibrated measuring cylinder. The
values of mass and volume were used to calculate
the density in grams per cm3 of each clam (Muller,
1967).
Ontogenetic changes in the morphometrics of
clams were analyzed with univariate linear regressions between width, height and density against
length for each coast. Departures from isometric
growth, i.e. intercepts different from zero (Gould,
1966), were tested with Student T-tests and differences in the rate of allometric growth, i.e. regression
slope, were tested with F-tests (Sokal & Rohlf 1981).
In order to characterize the shell shape of each clam
we calculated several dimensions of the shell as
ratios, or percentages, of shell length (Eagar, 1978) as
follows:
1) Width/length = clam wedge shape (where W/L
= 1 indicates a globose and W/L = 0.11 a blade
wedge);
2) Width/height = clam obesity or thickness
(where W/H = 1 indicates a thick and W/H = 0.33
thin or flat body);
3) Height/length = shell elongation (where H/L =
1 indicates a circular or round and H/L = 0.33 an
elliptical or elongated shell)
Shell shapes were then compared by plotting the
mean W/H against mean H/L ratios (modified from
Stanley, 1970) for the following class sizes from each
coast: 0-1.5 cm (recruits), 1.5-3.0 cm (juveniles),
3.0-4.5 cm (subadults)and> 4.5 cm (adults). Ontogenetic differences in shape and density were tested
with the Kruskal-Wallis test. Differences in morphometrics for each ontogenetic class between the two
coasts were tested using the Mann-Whitney U test
with the Z transformation for samples larger than 20
(Sokal & Rohlf 1981).
In order to test if differences in shell shape and
density are environmentally or genetically controlled, we compared adult clams from different
habitats on two southwest beaches only 50 km apart,
i.e. Silver Sands and Hermanus (Frg. 1). For these
comparisons we also applied the Mann-Whitney U
test. Following the results of Lombard & Grant
(1986), who showed that there is a high genetic
exchange between bivalve intertidal populations in
this region, we assume that these two nearby Donax
populations also exchange genes; thus, any significant
A.G. SOARES, R.K. CALLAHAN & M.C. DE RUYCK
410
differences in morphology or density between these
two populations are assumed to be habitat determined. Density determination on these populations
were based on shell measurements only. Data for
these analyses come from Soares et al. (1996), where
detailed information about the physical environment
and clam zonation on the southwest beaches can be
found.
RESULTS
Physical environment
Maitlands and Silwerstroomstrand were clearly
in a dissipative state, with a wide and gently
sloping intertidal zone (Table 1) and surf zone.
Sundays River beach was visually classified as
high energy dissipative state (Table 1). A storm
occurred prior to sampling this beach and large
waves eroded the subaerial profile, flattening
the slope and increasing the surf zone width.
Bloubergstrand had a steep profile and was in a
low-energy state.
Analyses for all beaches showed a trend for
grain size to decrease down the slope. Most
stations on the southeast coast beaches were
classed as medium-grained sand (i.e. 0.25-0.5
mm diameter) being on average finer than the
west coast beaches (Table 1). This is because
the west coast beaches had a number of coarsegrained stations with grains varying from 0.5
to 1.0 mm in diameter. This is surprising for a
dissipative beach such as Silwerstroomstrand,
which by definition should have fine sands
(Wright & Short, 1984). The coarse sand at
Silwerstroomstrand was probably caused by
erosion of the finer material from the beach
during the winter storms. The coarser sands
exposed by erosion associated with the long
wave periods generated by offshore storms
decreased the Dean's index of all beaches,
causing the dissipative beaches to fall in the
intermediate category (Table 1). As expected,
temperatures on southeast beaches were
higher than on west coast beaches (Table 1).
Clam size—zonation
The distribution of both adult and juveniles of
Donax serra differed significantly between the
west and southeast coast beaches (Fig. 2; F =
139, P < 0.001, DF = 3, 995). For west coast
beaches, the slope of the regression between
size class and position on the beach was significant and positive, showing that, on average,
larger clams occurred lower downshore than
small clams. At Silwerstroomstrand (Fig. 2a)
there was a high abundance of small individuals high up in the intertidal zone, i.e. at 36-52 m
from the drift-line, with few clams found in
the mid-intertidal zone. Large individuals were
more abundant in the lower intertidal to
subtidal stations. The general pattern at Bloubergstrand (Fig. 2b) was similar to Silwerstroomstrand with smaller individuals higher
up in the intertidal and larger individuals
occurring progressively lower down in the
intertidal and shallow subtidal. On this beach, a
wide berm running from 9 to 40.5 m from the
drift line increased the slope of the foreshore
and narrowed the beach width (Table 1 and
Fig. 2). As a result, the Donax zone was
compressed to only 20 m across the intertidal
(Fig. 2).
Maitlands, on the southwest coast, showed a
reversed zonation pattern to that found on the
west coast beaches; larger individuals were
generally found at the mid-intertidal stations
(at 59-66 m from the drift line) with clams
becoming increasingly smaller downshore.
Recruits were found subtidally between 0.5 and
1 m depth. On this beach, recruits, juveniles
and subadults were spread over a much wider
zone than the adults. At Sundays River Beach,
no zonation pattern was distinguished, with
all sizes occurring at all tide levels (Fig. 2d).
This beach had the widest intertidal clam
zone, c.a. 62 m, with both adults and juveniles
being found at extreme high shore positions,
i.e. the storm drift line. This zonation is quite
unusual and is most probably associated
Table 1. Physical characteristics of west and southeast coast beaches
West Coast Beaches
Parameters
Wave Height (m)
Wave Period (s)
Sand grain size (mm)
1/slope
Dean's index
Water Temperature CO
Silwerstroomstrand
1.96
12.85
0.45
50
2.36
14
Bloubergstrand
0.94
7.55
0.43
30
2.03
14
Southeast Coast Beaches
Maitlands
Sundays River
1.98
15.53
0.38
2.36
13.6
0.39
29
34
2.32
17
3.07
15
DL
20
' • • • - .
40
40
Distance (m)
60
*
K
•;
1I
«
Distance (m)
60EL
80
EL
! [
1
1
i*
!
j
•
•
80
jy
*
. I* \J^
1
4-
4-
1
|
|
SL
100
j
,
i
I
|
\
100
SL
i
i
•
•
jr--0.38
r = 092
120
120
•—I
10
!
i
45—
•
•
-
-
•
|
-
i
I
i
-
10
|
Jj.
*!
|
I
1
•
t
d) Sundays Rrver
i
!
—
DL
45 —
b) Btou berg strand
•
•
iI
20
30
t
•
•1
Distance (m)
30
!
' •
.
. >
•
i
EL
•
-
t
•
-
50
1
50
!
•
60
60
SL
. i
t .-•
• •
•
002
SL
j •
*
J"
•
••
I. —
i I1
••
I i
If
1
40
r ""1
40
EL
1
Distance (m)
;,
I r," t
t
• :*
20
j
r = 0 67
#
j
*
70
Figure 2. Donax serra size-zonation on beaches of the west coast a) Silwerstroomstrand, b) Bloubergstrand and the southeast coast c) Maitlands, d) Sundays River.
The x axis represents the distance of the station from the high tide drift line (DL). r = coefficient of correlation, EL = effluent line (i.e. the position where the water
table outcrops on the beach surface), SL = upper limit of the sublittoral.
4.5
20
c) MaHlanda
45 —
a) Slrwerstroomstrand
O
O
O
tn
O
50
412
A.G. SOARES, R.K. CALLAHAN & M.C. DE RUYCK
with the storm which occurred the day before
sampling.
Clam morphometric comparisons between the
coasts
There was a considerable overlap in the ranges
of all morphometric parameters; in general, the
west coast adult clams attained greater maximum lengths, widths, heights, weights and
volumes (Table 2).
All morphometric relations for clam populations of both coasts seem to follow allometric
growth, since they deviated significantly from
isometry, i.e. all intercepts were significantly
different from zero (Table 3). The rates of allometric change of each morphometric variable
against shell length, i.e. slope of the regressions, were significantly different between
populations on different coasts (Table 3). The
southeast clams grew faster in width while the
west coast clams grew faster in shell height and
density. Since the intercepts of the regressions
width versus length and width versus height
were higher for southeast clams, both juveniles
and adults of this coast were, on average,
thicker than west coast ones. The intercepts
of the regressions height versus length and
density versus length, however, were lower for
west coast clams—therefore recruits from this
coast were less dense and with smaller heights
than juveniles of the south coast while the
reverse was true for the adults, i.e. higher densities and shell heights were found on the west
than on the southeast coast.
Ontogenetic changes in clam morphology
were thus significant on both coasts—all
morphometric variables changed allometrically
and positively with length (Table 3). Clam
density increased with shell length on both
coasts with recruits, juveniles and subadults
being on average less dense than adults
(Kruskal-Wallis test: H = 344, P < < 0.001, Df
= 3,1000). The shape of the shell also changes
Table 2. Donax serra morphometric variables: means and (ranges).
West Coast Beaches
Variables
Length
(cm)
Height
(cm)
Width
(cm)
Weight
(g)
Volume
(cm3)
n
Silwerstroomstrand Bloubergstrand
3.47
(0.75-8.14)
2.32
(0.42-5.36)
1.17
(0.17-2.94)
18.02
(0.03-79.29)
12.07
(0.06-52.00)
122
3.11
(1.14-7.91)
1.97
(0.63-5.35)
1.00
(0.26-2.96)
9.82
(0.11-75.22)
6.79
(0.10-52.00)
148
Southeast Coast Beaches
Maitlands
Sundays River
3.66
(0.76-6.70)
2.29
(0.41-4.40)
1.31
(0.19-2.61)
11.06
(0.03-47.81)
8.24
(0.04-34.00)
324
3.4
(0.90-6.19)
2.12
(0.42-4.00)
1.17
(0.17-2.48)
8.95
(0.06-39.85)
6.6
(0.10-28.00)
409
Table 3. Donax serra allometric growth on different coasts.
Regression
Width x Length
West coast
Southeast coast
Height x Length
West coast
Southeast coast
Width x Height
West coast
Southeast coast
Density x Length
West coast
Southeast coast
1
Equation (y = a+b x)1
FTest
W = -0.21 + 0.39 L
W = -0.31 + 0.44 L
0.996***
0.991***
239***
H = -0.19 + 0.71 L
H = -0.21 +0.68L
0.997***
0.996***
46***
W = -0.10 + 0.55 H
W = -0.17 + 0.64 H
0.997***
0.991*"
401***
D = 0.78 + 0.12 L
D = 0.95 + 0.09 L
0.707***
0.475**
11**
all a(s) and b(s) are highly significant (P < 0.001, T-tests); **P < 0.01; ***P < 0.001
MICROEVOLUT1ON IN DONAX SERRA
with age—as recruits and juveniles grow older
they change from blade to more wedge shape
(Fig. 3). These shape changes were significant
for both coasts (Table 3 and Fig. 3).
Significant changes in shell shape of clams in
the same ontogenetic stage were detected
between coasts (Table 4). West coast clams in
all ontogenetic stages, i.e. recruits, juveniles,
subadults and adults, were consistently and
significantly rounder, flatter and less wedge
shaped than southeast ones (Fig. 3), with the
exception of H/L in recruits (Table 4). Thus,
notwithstanding the differences in juvenile
clam zonation, the shape of juvenile clams on
both coasts followed the shape of their parental
population. As predicted above by the regression analyses, density was significantly lower
in high upshore west coast recruits, while for
juveniles differences in density were not significant at P = 0.05, but were at P = 0.10 (Z =
— 1.6). West coast low intertidal subadults and
subtidal adults had average densities significantly higher than mid to high intertidal clams
of the southwest coast (Table 4).
Comparing the two southwest coast populations on Hermanus and Silver Sands, the shell
shapes were not significantly different between
inter and subtidal adults (P > 0.05). By contrast, shell density was on average significantly
higher in subtidal than in intertidal clams,
1.0
Cylinder
413
3
i.e. 2.75 and 2.45 g/cm respectively (MannWhitney test: U = 3, P < 0.05, Df = 12).
DISCUSSION
The contrasting zonation of Donax serra on the
west and southeast coasts has been mainly
attributed to the position of the adults: subtidal
on the former and intertidal on the latter coast
(Donn, 1990b). In our study, juveniles also
exhibited a contrasting zonation between
coasts; recruits and juveniles occurred higher
upshore on the west and lower downshore on
the southeast coast, being more abundant in
zones with fewer adults (Fig. 2). This adultjuvenile contrasting zonation seems to be a
density-dependent response of recruits to the
presence of adults (Schoeman, 1997). Several
mechanisms were suggested to explain this
density-dependent relationship, such as adultlarval predation, competition for food (Soares
et al., 1996) and sediment disturbance by adults
(Schoeman, 1997).
The only beach which showed no class sizezonation was Sundays River. A storm a day
before sampling eroded the beach profile,
scattering all class sizes throughout the intertidal gradient. Although we didn't collect a
control sample before the storm, Donn, Clarke,
•
Southeast coast
•
West coast
Sphere
0.84
I
i
0.67
A
SA •
SA
j
0.5
R
'
•
FI
•1
J
"
A
•
"
Blade
n IT
0.33
Disc
0.5
0.67
0.84
1.0
H/L
Figure 3. Ontogenetic changes in Donax serra shell'shapes from the west and southeast coasts of South Africa.
W/H - width to height ratio (Kruskal-Wallis H = 605, P < < 0.001, Df = 3,1000), H/L - height to length ratio
(KruskaJ-WaJlis H = 684, P < < 0.001, Df = 3,1000). R = recruits, J = juveniles, SA = subadults, A = adults.
414
A.G. SOARES, R.K. C A L L A H A N & M.C. DE RUYCK
Table 4. Geographical differences in morphology of Donax serra
Ontogenetic stages
Variables
Recruits
W/L
H/L
W/H
density
Juveniles
W/L
H/L
W/H
density
Subadults
W/L
H/L
W/H
density
Adults
W/L
H/L
W/H
density
NS
West coast
Southeast coast
Mean (S.D.)
Mean (S.D.)
n = 73
0.25(0.01)
0.58 (0.02)
0.42 (0.02)
0.80 (0.30)
n = 80
0.28 (0.02)
0.60 (0.05)
0.46 (0.03
1.09(0.28)
n = 42
0.32 (0.02)
0.64 (0.03)
0.50 (0.02)
1.39(0.19)
n = 72
0.36 (0.02)
0.68 (0.03)
0.53 (0.03)
1.48(0.10)
n = 71
0.25 (0.03)
0.54 (0.03)
0.46 (0.05)
1.00(0.39)
n = 234
0.29 (0.03)
0.58 (0.03)
0.50 (0.04)
1.15(0.29)
n = 210
0.35 (0.03)
0.63 (0.03)
0.56 (0.04)
1.30(0.19)
n = 217
0.39 (0.02)
0.65 (0.02)
0.60 (0.03)
1.39(0.14)
Mann-Whitney test
-0.22 NS
-8***
-5.94*"
-3***
-3.72*"
-4.42***
-1.12***
-7.32*
-4.5"
-8.95*
-2.59*
-8.23*
-9.52*
-11.44
-5.37*
P > 0.05 ; • • P < 0.01; • * • P < 0.001
McLachlan & du Toit (1986) sampled the
same beach and observed a clam size-zonation
pattern typical for this coast, with juveniles low
and adults high intertidally. On the west coast,
Birkett (1986) observed the same scattering
phenomenon of clams after a storm, with the
difference that adult clams were scattered
subtidally. It would be interesting to monitor
D. serra zonation prior to and after a storm to
measure the zonation resilience, i.e. the time
necessary for clams to regain their normal
position across the shore. There is a wealth of
literature recording faunal zonation in general,
and size zonation in particular, on sandy
beaches, the number of zones being subject to
some polemics (reviewed by McLachlan &
Jaramillo, 1995). Since beach fauna is highly
mobile, it is easy to understand that biological
zones will follow the dynamics of the environment, contracting and expanding as the beach
builds up and erodes away. Thus, the fact that
biological zonation is not static does not imply
that it doesn't exist as claimed in recent studies
(e.g. Haynes & Quinn, 1995; Brazeiro & Defeo,
1996).
In marine molluscs there seems to be a very
good relationship between form and function,
with shell shape being adapted to the habitat
colonized (Kaufmann, 1969). One of the key
features of sandy beach fauna is to have high
mobility to migrate and burrow between
swashes. Sandy beach bivalves are the fastest
burrowers amongst the Bivalvia (Stanley, 1970;
McLachlan et al., 1995), small tropical Donax
burrowing as fast as 2 s (Ansell & Trevallion,
1969). Sandy beach donacids and mesodesmatids seem to have converged to a more
wedge shape, which is apparently an adaptation for swash-riding. A wedge shape increases
the drag, stability and orientation of the shell in
swash flow (Ellers, 1995). In wedge shaped
clams, maximum shell width in cross-sectional
outline usually occurs in the dorsal or posterior
region of the shell, opposite the site of pedal
emergence. This minimizes the cross-sectional
angle of the leading edge of the shell during
burrowing (Stanley, 1970).
In this study, all ontogenetic stages of west
coast D. serra had shapes significantly different
from those on the southeast coast: the former
were flatter and more round and the latter
were thicker and more wedge shaped. That is
the first time such shape differences are found
for ontogenetic stages other than adult clams.
Donn (1990a) in an attempt to explain the contrasting adult clam zonation between west and
southeast coasts, suggested that it is shell shape
which determines zonation and not the other
way around; he stated that clams occur subtidally on the west coast not only because of
MICROEVOLUTION IN DON AX SERRA
the reduced burrowing speeds caused by low
temperatures, but also because thin and round
clams burrow slower and swash-ride less efficiently than wedge shaped clams. Although it is
true that flatter clams, being more streamlined
than thicker ones, have lower drag and thus
need a stronger swash to be transported
(Ellers, 1995), they burrow deeper (Stanley,
1970) and faster (Trueman, Brand & Davis,
1966) than thick shelled clams. Additionally,
adult Donax serra are non-migratory on the
west coast (Brown, Stenton-Dozey & Trueman, 1989) weakening the shape-habitat
hypothesis.
We believe that different shell morphologies
of D. serra in different habitats are the result,
not the cause, of a directional selection (sensu
Grant, 1991) on adult clam shapes. This may be
exemplified by examining the distribution of
W/L in adult clams of each coast (Fig. 4).
Although the range of shapes is similar for
each coast, more than 90% of the southeast
coast clams are in the range of more globose
shells, i.e. 0.36-0.45, while 90% of the west
coast clams are in the range of more blade
shaped shells, i.e. 0.30-0.39 (KolmogorovSmirnov test: D = 0.59, P < 0.001, DF = 289).
This suggests that thick, wedge shaped shells
are selected against in the subtidal, while flat,
415
disc shaped shells are selected against in the
intertidal. To test this hypothesis we compiled
a table with the information from the literature
about shell shape and maximum length of 13
typical sandy beach bivalve species from the
Donacidae and Mesodesmatidae (Table 5). At
the species level, subtidal clams are significantly thinner, or more blade shaped, than intertidal ones (Student T test: T = 2.94, P < 0.05,
Df = 11). Furthermore, subtidal forms are on
average larger than intertidal ones (Student T
test: T = -3.06, P < 0.02, Df = 11). These size
differences have also been observed in Donax
serra by several authors (Donn, 1990a; Soares
etal., 1996) and in this study (Table 2). Smaller
and more wedge shaped clams are most
probably selected for in the intertidal because
they both burrow faster and swash-ride more
efficiently than large and thin clams. High
desiccation rates and predation by ghost-crabs
(Smith, 1971) and birds (Ward, 1991) may
play a role, selecting against the unsuccessful
burrowers stranded higher upshore. Although
larger clam size in the subtidal may have a
non-adaptive explanation, i.e. reflecting longer
periods of feeding (Soares et al. 19%) and/or
higher food productivity (Soares, Schlacher &
McLachlan, 1997), the heavier and denser
shells do increase stability in the sediment
0 27 0 30 0.33 0.36 0 39 0.42 0.45
0.27 0.30 0.33 0.36 0.39 0.42 0.45
W/L
Southeast
West
Figure 4. Distribution of W/L, width to length ratios in subtidal adult clams of the west coast and intertidal
adult clams of the southeast coast. Arrows point to shapes which were selected against, i.e. had their percentage decreased, on each coast.
416
A.G. SOARES, R.K. CALLAHAN & M.C. DE RUYCK
Table 5. Size and wedge shape (W/L) of Donacidae (D) and Mesodesmatidae (M) in different sandy
beach habitats.
Species
Intertidal
Donacilla angusta (M)
Donax variabilis (D)
Donax faba (D)
Donax denticulatus (D)
Donax hanleyanus (D)
Atactodea striata (M)
Average
Subtidal
Mesodesma mactroides (M)
Mesodesma donacium
Paphies subtriangulata (M)
Mesodesma arcatum
Paphies donacina (M)
Donax sordid us (D)
Iphigenia brasiliensis (D)
Average
Donax sarra (D)
Intertidal
Subtidal
Maximum
length (cm)
W/L
Shape
Source
2.3
2.3
2.4
3
2.4
3.6
2.7
0.329
0.372
0.392
0.447
0.47
0.496
0.416
blade-wedge
wedge
wedge
globose-wedge
globose-wedge
globose
globose-wedge
McLachlan etal.
Ellers 1995
McLachlan etal.
Stanley 1970
McLachlan etal.
McLachlan etal.
-
7.6
6.1
>10.0
3.5
>10.0
2.2
6
6.5
0.263
0.274
0.327
0.34
0.349
0.394
0.422
0.338
blade-wedge
blade-wedge
wedge
wedge
wedge
wedge
globose-wedge
wedge
McLachlan etal.
McLachlan etal.
McLachlan etal.
Stanley 1970
McLachlan etal.
McLachlan etal.
Stanley 1970
-
6.7
8.1
0.382
0.361
wedge
wedge
present study
present study
(Stanley, 1970) and probably also provide a
size-refuge from fish predation. These patterns
are, however, not a rule for all sandy beach
bivalves, with small (Kilburn & Rippey, 1982)
and/or globose (McLachlan, Dugan, Defeo,
Ansell, Hubbard, Jaramillo & Penchaszadeh,
1996) clams occurring in the low inter to subtidal. The occurrence of large intertidal Donax
serra on the southeast coast is also at variance
with the size-habitat hypothesis. Thus, in
certain cases, selection of size and shapes may
be phylogenetically constrained by what
phenotypes are available. In these species, life
history features such as high larval output
associated with long life spans (McLachlan et
al. 1996) and rapid growth (Schoeman, 1997)
do increase fitness, counteracting the apparent
lack of adaptedness in size or shape.
It is well known that there is a latitudinal
gradient of increasing body size in higher
latitudes for several species of endo- and
ectotherms (Vermeij, 1978). This is generally
attributed to physiological constraints of lower
temperatures that decrease growth and maturation rates (Atkinson & Sibly, 1997) providing
a non-adaptive explanation for the latitudinal
gradient in body size. However, molluscs tend
to grow bigger and have thicker shells in the
tropics than in polar regions; this is because of
the lower solubility of calcium carbonate and
higher solubility of carbon dioxide in warm
1995
1995
1995
1995
1995
1995
1995
1995
1995
waters, both facilitating calcium absorption and
shell growth (Vermeij, 1978). In Donax serra,
although cold water west coast clams grow to a
bigger size than the warm water southwest
clams, both populations have a similar rate of
individual growth (Schoeman 1997). Also,
Weinberg & Helser (1996) noticed that the surf
clam Spisula solidissima may grow faster in
colder waters. It seems that the non-adaptive
developmental temperature-size hypothesis
does not apply to beach clams. Differences in
clam sizes on sandy beaches may be explained
by differences in food productivity (Soares et
al., 1997), feeding periods (Soares et al., 1996)
or mortality rates caused by either predators
(Ward, 1991; Gibson, Robb, Burrows & Ansell,
1996) or disturbance factors (Ansell, Robb &
Powell, 1988).
Three lines of evidence in the present study
point to the environmental control of shell
density: i) subtidal west coast adults of D. serra
had higher densities than the intertidal ones on
the southeast coast, ii) intertidal shells were on
average less dense than subtidal ones on
beaches of the same coast and iii) high intertidal recruits of the west coast had a lower
density than low intertidal ones on the southeast coast. Intertidal molluscs undergo anaerobic metabolism during exposure to air,
lowering the tissue pH to acidic levels which in
turn decalcifies the shell and decreases its
MICROEVOLUTION IN DONAX SERRA
density (Vermeij, 1978). Intertidal Donax serra
rely heavily on anaerobic metabolism as a way
to save energy (Cockcroft, 1990), suggesting
that decalcification of the shell may occur in
intertidal populations.
Density has been claimed to be a key parameter in determining which bivalve species can
colonize different beach types (McLachlan et
al., 1995). Two roles have been suggested for
density: higher density seems to confer stability
during swash-riding (Ellers, 1995; McLachlan
et al. 1995) and to increase stability of the clam
within the sediment (Kaufmann, 1969; Stanley,
1970). Adult D. serra is not migratory on the
west coast, thus higher densities and heavier
shells in subtidal populations may increase
stability in the sand and aid burrowing in the
shifting sediments of the turbulent surf zone.
Conversely, intertidal adult clams of the southeast coast do undergo semi-lunar migrations
(Donn et al., 1986) and have lower densities.
Finally, the lowest shell densities are found in
recruits, which are highly migratory (Donn,
1987) and easily transported by waves (pers.
obs.). Thus, for D. serra density is negatively
correlated to mobility, supporting the role
advanced by Kaufmann and Stanley. Ansell
(1985), studying 4 species of Donax from Hong
Kong beaches, also observed an inverse correlation between mobility and density.
The ontogenetic differences in shell shape
and density all seem to be adaptive; clams with
thinner, smaller and less dense shells burrow
faster and are more easily transported than
clams with heavier, larger and thicker shells
(Stanley, 1970). These features explain the
higher mobility of juvenile D. serra across
(Donn et al., 1986) and along shore (Donn,
1987) which most probably enhances the postsettlement dispersion of the species along the
extensive beaches found in South Africa.
Although the juvenile D. serra occupied different zones on both coasts, their body shape
followed the trend of their parental adults and
not the one which would be expected by the
shape-habitat relationship suggested by Donn
(1990a). This indicates that shape selection is
stronger in the adults and is inherited by
juveniles and reflected in their shapes. Further
evidence for the genetic control of morphological variability is given by the two adult populations inhabiting the same coast but different
habitats—they showed no significant difference in body shape, probably because there is
genetic exchange between those two populations on the southwest coast; this hypothesis
is in agreement with the absence of genetic
417
differences in Choromytilus populations of this
region (Lombard & Grant, 1986). This may
indicate that the selection pressure on the
shape of sub- and intertidal D. serra works on
evolutionary rather than ecological time scales.
Alternatively, the small clam populations on
this coast may favour genetic drift (Grant,
1991), preventing the selection for different
shapes to be fixed in those populations. Morphologic differentiation between sympatric
Donax species is generally accompanied by
genetic (Nelson, Bonsdorff & Adamkewicz,
1993, Adamkewicz & Harasewych, 1994) and
niche distinctiveness (Ansell, 1985).
The notion that marine populations with
planktotrophic larval development will have
a much higher genetic connectivity than populations with direct development is widely
accepted (Murray-Jones & Ayre, 1997 and
references therein). Genetic connectivity between populations geographically widely separated, such as those studied here, is only
possible if the current system is appropriate
and larval life is long enough to allow transport
and settlement in the other area. Using an
average westwards current velocity of 0.31 m/s
occurring 51.2% of the time (Harris, 1978), a
D. serra larva released in Maitlands, in the
southeast coast, during summer would take a
minimum of 86 days to travel the 1181 km of
coast and reach a west coast beach. This is
much longer than the 4 weeks period of larval
development (D. Schoeman pers. comm.).
Considering that i) the Benguela current is
deflected 300-400 km offshore around Cape
Agulhas, and ii) during 19.5% of the time, on
average, eastwards currents prevail (Harris
1978) reversing the direction of coastal plankton transport, a larva would take an infinitely
longer time than its life span in the plankton to
get to the west coast. The stepping stone model
of genetic connectivity (Murray-Jones & Ayre,
1997) is an improbable mechanism of linking
southeast and west D. serra populations, since
population sizes in between those two coasts
are too small (Schoeman, 1997) to generate a
surplus of larvae necessary to repopulate other
geographic areas. We, thus, expect some
genetic differentiation to occur between southeast and west coast populations as a result of
the low/null geneflowbetween them. A genetic
study on several adult populations distributed
along these two coasts would certainly shed
light on this question.
Donax serra appeared 5 million years ago in
the fossil records of the late Miocene to early
Pliocene, simultaneously on both west (Kensley
A.G. SOARES, R.K. CALLAHAN & M.C. DE RUYCK
& Pether, 1986) and southeast coasts (Le Roux Any organism living in such unstable environ1993). By that time, there were infrequent ment should be able to adjust itself to cope
tongues of coastal upwelling on the southwest with these constantly changing conditions.
coast and the climate was intermediate Indeed, beach fauna have a high behavioural
between the subtropical mid-Miocene and the (De Ruyck, McLachlan & Donn, 1991; Brown,
present—the water temperature was probably 1996), morphological (Wade, 1967; Weinberg
higher than nowadays (Shannon, 1985). Since & Starczak, 1989; Donn, 1990a; this study)
the subtidal adult clam zonation seems to be and ecophysiological plasticity (Dexter, 1977;
related to lower temperatures (Donn, 1990a) Stenton-Dozey & Brown, 1994). Probably, in
and a disturbance effect caused by stranding changing environments plastic species survive
kelp (Soares el al. 1996), both associated with longer than non-plastic species over evolutionthe present coastal upwelling, we hypothesize ary times. This is in agreement with the hypothat Donax serra was primarily intertidal on
thesis that stasis (i.e. lack of speciation)
both coasts in the Miocene-Pliocene. In the predominates in changing environments while
Pliocene, there was a dramatic decrease in phyletic gradualism (i.e. speciation) predomitemperature which enhanced the frequency nates in stable, narrow-fluctuating environand intensity of southeasterly winds, triggering ments (Sheldon, 1990). Plasticity may, therefore,
the establishment of the Benguela coastal increase species adaptability and survival in
upwelling system by the early Pleistocene, c.a. changing environments such as sandy beaches
2 million years ago (Shannon, 1985). During over ecological and evolutionary time scales.
this period, the west coast adults of D. serra In this context, morphological (density) and
probably assumed a subtidal position while the ecophysiological plasticity seem to have enabled
southeast populations kept their original inter- D. serra to survive the intense temperature and
tidal positions. Other large Donax species, now sea level fluctuations characteristic of the Mioextinct, were contemporaneous with D. serra in cene to Pleistocene, and to establish populathe Pliocene and Pleistocene, i.e. D. haughtoni, tions in different beach habitats along 2000 km
D. rogersi and D. sanctuarium on the west of coast.
coast and Donax sp on the southeast coast
(Carrington & Kensley, 1969; Kilburn &
Tankard, 1975; Le Roux, 1993). There is some
CONCLUSIONS
evidence which suggests that lack of morphological and/or physiological plasticity may
explain the extinction of these species. D. Observed differences in shell shape of Donax
rogersi, a large and thick shelled species, is serra between the west and southeast coasts are
claimed to have replaced D. haughtoni, a likely to be the result of a directional selection
smaller and thin shelled species with little process acting on adult clams. Selection, in this
morphological variation, because of lack of case, is imposed by the habitat colonized and
morphological adaptation of the latter to the occurs over evolutionary time. The subtidal
accumulation of coarser sediments in the early habitat selects for characteristics which decrease
Pleistocene (Carrington & Kensley, 1969). transport, i.e. non-migratory behaviour, blade
Also, D. haughtoni is absent in areas where the to disc shaped shells, and improve stability
waters are colder than the ones where the in the sediment, i.e. large, heavy, and dense
species normally occur (Tankard, 1975c in bodies. By contrast, the intertidal habitat
Kensley & Pether, 1986) suggesting a steno- selects for characteristics which improve
mobility, i.e. migratory behaviour, more wedge
topic physiological adaptation.
shaped shells, smaller, lighter and less dense
Beaches are considered one of the most bodies. The microevolutionary changes in shell
dynamic environments on earth (McLachlan, shape are probably maintained by low or null
1990). They are subjected to daily variation in genetic exchange between these geographically
moisture levels and temperature during tidal isolated populations. Differences in shell
cycles, seasonal variation in wave climate with density between sub- and intertidal clams seem
stormy and calm periods and also high erosion to be a physiological response to the habitat
and deposition rates (Bascom, 1964). Beaches colonized, most probably occurring over short
also vary spatially and temporally in morpho- ecological time spans. Shell density, being
dynamics, ranging from reflective states, with inversely correlated to mobility, has functional
steep slopes, short swashes and coarse sands, to value and probably improves survivorship on
dissipative conditions with flat slopes, long sandy beaches.
The ontogenetic changes in shape are, preswashes and fine sands (Wright & Short 1984).
418
MICROEVOLUTION IN DONAX SERRA
419
sumably, adaptive in this species: larger, ATKINSON, D. & SIBLY, R.M. 1997. Why are organisms usually bigger in colder environments?
thicker and denser shells increasing stability of
Making sense of a life history puzzle. Trends in
the adults in the sediment and smaller, thinner,
Ecology and Evolution, 12: 235-239.
and less dense shells increasing mobility and
BASCOM,
W.N. 1964. Waves and beaches. The dynamdispersion of juveniles.
ics of the ocean surface. Anchor Books, New York.
Phenotypic plasticity in present D. serra BIRKETT, D.A. 1986. Apparent fluctuations on the
populations is suggested to be an important
distribution pattern of Donax serra on the west
factor enhancing the survivorship of the species
coast. In: Biology of the genus Donax in Southern
over ecological (i.e. biogeographic, habitat)
Africa (T.E. Donn, ed.), 30-33. Reports of the
institute for Coastal Research, University of Port
and evolutionary scales.
Elizabeth, Vol. 5.
BRAZEIRO, A. & DEFEO, O. 1996. Macroinfauna
ACKNOWLEDGEMENTS
We would like to thank Alec Brown, Dick Kilburn,
Dave Schoeman and Thomas Schlacher for valuable
comments which greatly improved the manuscript.
We appreciate the help of Joseph Sara and Ad61e
Hattingh with the field work along the south-east
coast and Ronel Nel and her team on the west coast.
Thanks go to Anton McLachlan for transporting
samples from Cape Town. Andrt: Vorster analyzed
the sediment and Alison Callahan assisted with
laboratory work. Roger Langohr kindly provided
facilities at the University of Gent (Belgium) during
the writing of this paper and Dan Baird provided
research funds at UPE. A.G.S. was supported by a
grant from the Brazilian Council for Science and
Technology (CNPq).
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